A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading

1In the last 20 years, there has been an explosion of research into the neural basis of language processing. This has clearly established that spoken and written language relies on concurrent activation in multiple brain areas. The location of these regions has been identified with functional neuroimaging techniques such as Positron Emission Tomography (PET) and functional Magnetic Resonance Imaging (fMRI) that measure hemodynamic changes, while the timing of brain activity during language processing has been identified using electromagnetic techniques such as magnetoencephalography (MEG) and electroencephalography (EEG). Although it is the combination of these spatial and temporal measurements that is needed to provide a mechanistic account of language, the current review focuses only on the localisation of language and reading areas with PET and fMRI.

2Prior to the availability of functional imaging techniques, our understanding of language in the brain rested on studies of impairments in patients with brain damage or patients undergoing electrical stimulation during neurosurgery. The most popular neural model of language was based on the writings of Broca, Wernicke and Lichtheim at the end of the 19th Century and Geschwind in the mid 20th Century. Auditory speech recognition was localized to the left posterior temporal cortex (Wernicke's area); speech production (motor word representations) was localized to the left posterior inferior frontal cortex (Broca's area); and visual word recognition was localized to the left angular gyrus. One of the major limitations with this classical neurological model is that it does not indicate how single words are combined into meaningful sentences. This was highlighted in the latter half of the 20th Century, when it was noted that although Broca's aphasics could comprehend heard speech based on semantic content, they had difficulty comprehending sentences that depended on complex syntactic analysis. It was also noted that circumscribed damage to Broca's area only resulted in temporary speech production difficulties and that permanent speech production difficulties were observed when frontal lobe damage extended into the insula and parietal regions in patients with left middle cerebral artery infarcts.

3The neurological model of language also failed to explain why those with reading difficulties might have a selective impairment of the ability to read whole words with atypical spellings such as “yacht” or, conversely, a selective impairment of the ability to read nonwords with no meaning such as “yatched”. Such observations suggested that there are two or more different pathways to speech output from text. The complexity of language processing and the importance of many regions outside Broca's and Wernicke's territories were therefore well appreciated prior to the availability of functional imaging techniques such as PET and fMRI.

4The landmark of functional imaging study of auditory and visual word processing was published in 1988 by Petersen and colleagues who used PET to identify the brain areas activated when healthy participants were presented with auditory or visual single words and were instructed either to view them passively, repeat them or generate a verb that was related to the heard or seen noun (e.g. “eat” in response to “cake”). On the basis of the results and other deductions, the authors concluded that (i) auditory word forms were processed in the left temporoparietal cortex, (ii) visual word forms were processed in the left extrastriate cortex, (iii) semantic associations involved the left ventral prefrontal cortex, (iv) word generation involved the dorsolateral prefrontal cortex; (v) general response selection involved the anterior cingulate; (vi) articulatory coding and motor programming involved the left ventral premotor cortex, left anterior insula (referred to as the buried sylvian cortex) and supplementary motor cortex (SMA) and (vii) motor execution involved the rolandic cortex (the posterior part of the precentral gyrus bordering the central sulcus). Together the results provided a new anatomical model of lexical processing that is illustrated in Fig. 1. The key features of this model were the inclusion of a small number of discrete areas with multiple parallel routes between localized sensory-specific, phonological, articulatory and semantic-coding areas.

5Shortly after this study, the same authors published a PET study of reading that compared regional activation in response to visual words and word-like stimuli. The association of the left medial extrastriate cortex with visual word form processing was confirmed because this area was activated by visually presented words and pseudowords that obey English spelling rules but was not activated by unfamiliar strings of letters or letter-like forms. In addition, activation in the left frontal cortex which had been associated with semantic processing during word generation was found to be more activated by passive presentation of words than pseudowords. Thus were able to distinguish high-level visual and semantic computations on single words and describe the underlying anatomy.

6In 1991, Petersen and colleagues' early findings were replicated and extended. found that the response in the left posterior superior temporal cortex (Wernicke's area) dissociated from that in other left and right superior temporal regions because only activation in the left posterior temporal area was independent of the rate of presentation of the auditory input. The importance of considering how frontal and temporal lobes interacted was highlighted by who demonstrated that when words were produced without stimuli (i.e. verbal fluency) activation increased in the left dorsolateral prefrontal cortex but decreased in superior temporal cortices, whereas, during lexical decisions on heard words, activation increased in the superior temporal cortices with no change in prefrontal activation. In a follow up paper, the same authors pursued the emphasis on regional interactions by correlating activation in the superior temporal gyrus and prefrontal cortex and proposing that word representations were distributed in the left superior temporal cortex and word processing in the temporal lobe was modulated by the left dorsolateral prefrontal cortex.

7The importance of these early PET studies was far reaching. They illustrated that functional imaging could provide anatomical localization with a precision that far exceeds that attainable with human brain lesion studies. Moreover, the study of healthy subjects avoids possible confounding effects of brain lesions, such as compensatory reorganization of brain function. Methodological challenges were also well appreciated particularly when the results appeared to contradict classic axioms of language organization. For example, argued that data should not be averaged over subjects because intraoperative stimulation showed diversity in location of language functions and morphometrical imaging studies showed diversity of brain shape and gyral patterns that would be difficult to correct with anatomical normalisation techniques. Many other concerns were succinctly addressed in a review by who pointed out that functional neuroimaging results should be viewed as evolutionary, rather than revolutionary and that they were most interpretable when they were backed up by supporting data from other studies. For example, after the, Petersen et al. (1989) observation that the right lateral inferior cerebellum was activated by cognitive rather than sensory motor computations, they demonstrated that damage to the right cerebellum impairs practice related learning and detection of errors. also emphasized that complex language functions were not localized in specific brain regions; they were distributed across networks of regions with each area making a specific contribution to the performance of the task which depends on its connections to other areas in a parallel distributed hierarchy. In this context, understanding the functional anatomy of language cannot be deduced from a single experiment; rather, it requires the integration of results from multiple experiments using multiple techniques.

8The first fMRI studies of language processing were reported by,, ), and. The results provided a reassuring demonstration that fMRI could replicate the findings of PET. For example, showed that word generation, relative to repetition, activated the inferior frontal cortices and anterior insula as previously reported using PET, while and illustrated that increasing the rate of presentation of simple auditory speech stimuli resulted in a monotonically proportional increase in bilateral superior temporal lobe activation, as previously reported using PET. As fMRI became more available, functional imaging studies of language could be conducted on children and females of childbearing age who had previously been excluded because of the risk of the radiation dose involved in PET scanning. As fMRI is a non-invasive procedure, the same subject could be scanned multiple times thereby providing robust data from individual subjects and this opened the way for studies of inter-subject variability.

9This review focuses on papers, reported between 1992 and 2011, that aimed to identify the brain areas activated when healthy adults were engaged in speech comprehension and production tasks. Papers were selected from PubMed if their titles or abstracts included a specific combination of search words. One search word would be a language process of interest (e.g. semantics, phonology, comprehension, articulation, etc.) while the other search word would be either an imaging term (e.g. fMRI, PET or functional imaging) or a brain region (e.g. SMA, cerebellum). Papers were excluded if: (a) their aim was to infer language processing from brain activation (as opposed to reporting brain activation in response to language processing), (b) their conclusions were about abnormal populations (e.g. in dyslexics, schizophrenics, stroke patients etc.) and (c) they reported activations that varied across normal populations (e.g. due to age, gender, ability etc.). This was not from lack of interest but due to the time frame for writing the review and the overwhelming number of papers (> thousand) that needed to be considered. The papers identified are also influenced by my personal memories of how our knowledge unfolded over the past 20 years, the availability of papers on PubMed, the choice of search terms used by me and the key words used by the authors.

10For each paper, I extracted the conclusions stated in the abstract; and made minimal adjustments to the functional and anatomical terms. I only changed terminology that was inconsistent with that used in other studies. For example, the terms Broca's area, BA 44, inferior frontal cortex and pars opercularis have been used interchangeably. I chose pars opercularis to make a clear distinction with other frontal regions, such as the pars orbitalis, pars triangularis and premotor cortex. Contrary to my previous review and methodology used in computational meta-analyses (e.g. ), the conclusions are not based on the standard (Talairach or MNI) co-ordinates of peak activations. The disadvantage of not using a co-ordinate based meta-analysis is that the conclusions depend on the subjective interpretation of the authors. However, computational meta-analyses based on reported co-ordinates are also subjective because they depend on the statistical threshold used by the authors, the sensitivity of the paradigm (conditions and number of participants), the precision with which the co-ordinates describe the extent of the activation, and the inclusion criteria of the meta-analysis. The methodology used in the current review has the advantage of being able to report (a) conclusions drawn by authors who controlled the collection of the data; and (b) a historical perspective of how and when the conclusions emerged.

11The reporting of results is structured around three sections that focus on auditory speech comprehension, speech production and reading. Within the auditory speech section, the subsections focus on auditory responses that do not distinguish speech from nonspeech; auditory responses that are greater for speech than nonspeech; and comprehension of speech at the word and sentence level. Within the speech production section, the subsections focus on word retrieval, covert articulatory planning, overt articulation and post-articulatory sensorimotor feedback. Within the visual word processing section, the subsections focus on responses that distinguish visual words from other visual stimuli and differences between the lexical and sublexical mapping of orthography (letter combinations) to phonology (sounds).

12To demonstrate the progressive steps in the evolution of our knowledge, I have further divided each subsection into 4 time era according to the year of publication. These are (i) 1992–1996 when PET was in its heyday and the contribution of fMRI was being validated; (ii) 1997–2001 when fMRI was taking over; (iii) 2002–2006 when there were notable improvements in the spatial definition of language areas; and (iv) 2007–2011 when there were many further refinements as well as a much greater focus on using functional anatomy to test cognitive models of language. Within each of these time era, I have also attempted to dissociate novel conclusions from replicated conclusions.

13The results of the review are reported in relation to the functional–anatomical model from which is illustrated in Fig. 1. This was edited to provide more functional terms (Fig. 2) and the anatomical attributions associated with these functions (Fig. 3). Fig. 4 provides a sketch of the left hemisphere anatomical locations of the activations related to different language-related functions, after rendering activations from my own data onto a canonical model of the left hemisphere. Table 1 defines the functional terminology used in Fig. 2. Table 2 provides a historical perspective of the anatomical attributions according to the time era in which they emerged. Table 3 provides the full anatomical names of the abbreviations used in Table 2. Table 4 reverses the inference in Table 2 by listing the anatomical regions in alphabetical order for easy reference to the language functions identified in the review. The studies that contributed to the review and my synthesis of its findings are provided in the Discussion.

14This section is included because studies of auditory responses that are not specific to speech sounds have provided important clues for understanding how speech processing emerges. For example, “left lateralized” nonspeech processing may be a precursor to left lateralized higher-level language functions.

15One of the most surprising early findings was that the planum temporale (on the dorsal surface of the superior temporal gyri and the ventral surface of the sylvian fissure) showed similar responses to heard speech and tones. This finding suggested that both the left and right planum temporale were involved in early auditory processing, which is contrary to the classic view that the left planum temporale was specialised for language. An equally surprising finding was that the left planum temporale was activated in the absence of any auditory input: for example, during silent speech production and when subjects imagined hearing another person's voice. This suggested a special role for the planum temporale in higher-level auditory representations that could be tapped by bottom up processing of auditory inputs or top-down processing of learnt auditory images.

16Further evidence was reported that the left planum temporale was involved in silent auditory imagery of speech or when recalling (imagining) the auditory relative to visual associations of a picture of a scene.

17Functional subdivisions were described within the bilateral auditory cortices with simple auditory stimuli activating the transverse temporal gyri (BA 41), sounds with discontinuous acoustic patterns activating the surrounding superior temporal gyri (BA 42), and sounds with complex spectral intensity, and temporal structures (heard words and music) activating areas that extended into the bilateral superior temporal sulci (BA 21, 22). also noted that anterior regions in bilateral superior temporal cortex were particularly sensitive to variation in the spectral content of nonverbal stimuli.

18Left lateralized responses to nonspeech sounds were identified in the auditory cortex (superior temporal gyri) by when participants listened to nonverbal sounds containing rapid relative to slow frequency transitions. As rapid frequency modulations are a key feature in speech sounds, the observed left lateralization was proposed to contribute to the lateralization of higher-level language functions.

19Beyond the temporal lobes, speech and nonspeech sounds activated the left inferior frontal cortex (pars triangularis and pars opercularis) when they needed to be segmented and held in auditory working memory. This is important for appreciating that left inferior frontal activation during auditory speech processing does not necessarily indicate a speech specific function.

20Many studies observed activation in bilateral dorsal superior temporal cortices during early auditory processing of both speech and nonspeech sounds with increased activation when acoustic complexity increased, the rate of word presentation increased, when the listener had to segregate two simultaneously presented speech sounds, for the perception of distorted speech sounds, for hearing syllables relative to vowels and for auditory speech in noisy environments.

21Auditory imagery of the sounds was again associated with left lateralised activation in the planum temporale in response to experience with tones and visual stimuli, in the silence that followed familiar music even when there was no instruction to remember the music, when passively viewing finger tapping on the piano following keyboard training, when producing rhythmic finger sequences that had been learnt with an auditory cue and when imagining heard speech, music or environmental sounds in the absence of sound.

22The view that left lateralization for heard speech might arise at the level of detecting rapidly changing temporal features was strengthened by observations that posterior temporal activation was left lateralized for rapid relative to slow frequency transitions and for broad relative to narrow band speech envelope noises. Alternative hypotheses were that left lateralization in both temporal and inferior frontal areas were related to a top down attentional bias or auditory-motor processing.

23Right lateralized auditory responses were observed for environmental sounds, non-linguistic vocal sounds like laughter, and the familiarity of vocalisation. These right hemisphere responses may help to explain why the perception of prosody in heard speech prosody is associated with the right hemisphere, particularly when the language demands of the task are low.

24Bilateral superior temporal activation was reported for the acoustic analysis of speech and nonspeech sounds and shown to be sensitive to frequency discriminations, familiarity, spectral structure and temporal modulation.

25Left lateralized responses were reported for the discrimination of fast changing verbal and nonverbal sounds in the planum temporale and for the perceptual interpretation of speech sounds in early auditory areas. In contrast, right auditory areas were associated with changes of the frequency spectrum, categorical perception of familiar musical chords, and the comparison of familiar versus unfamiliar musical sequences, spectrally rotated speech sounds compared to speech masked by noise and rhythm and intonation in nonspeech. This provided further support for the importance of right superior temporal activation in the prosodic processing of speech which relies on detecting variations in the frequency spectrum, rhythm and intonation.

26The association of the planum temporale with auditory imagery during silent production tasks (e.g. silent humming) was replicated but complicated by multiple reports that the posterior planum temporale (on the dorsal surface of the posterior superior temporal gyrus) and the surrounding temporoparietal cortex were activated under a wide range of conditions including visual stimuli without auditory stimuli or auditory associations. In addition, activation in the planum temporale was reported during phonation and exhalation, auditory working memory and for syntactic processing of auditory and written sentences.

27The multi-functional responses reported in the posterior planum temporale may have resulted from conflating different functional regions. For example, the practice of functionally defining a region of interest that is commonly activated by auditory inputs and covert articulation might artificially merge distinct auditory and motor regions in the ventral and dorsal surfaces of the sylvian fissure particularly when data are smoothed and averaged over subjects. A second possibility is that, within the same temporoparietal region, there are multiple overlapping functionally distinct cell populations for perception and covert production.

28A third explanation of common responses to auditory, motor and memory processes in the same anatomical area is that they reflect a common process. For example, activation during auditory working memory, silent motor tasks and sentence processing can all be explained by the demands on auditory imagery. Models of visual processing provide a useful analogy here because it has been shown that early visual cortices (e.g. the calcarine cortex and the lateral occipital cortex) are activated during visual imagery in the absence of visual stimulation with this early sensory activation sustained by recurrent interactions with higher-level processing areas. Future studies are therefore needed to provide a more precise definition of the functional responses in both the left posterior planum temporale and the left ventral supramarginal gyrus during auditory processing.

29Auditory processing of speech and nonspeech sounds activates the bilateral superior temporal gyri (STG in Table 2 and Fig. 3) that include and surround Heschl's gyri. Three observations relevant to higher-level speech processing have been described. First, left lateralized superior temporal activation during auditory processing has been observed and related to hemispheric differences in the processing of rapidly changing auditory inputs and/or the influence of left lateralized inferior frontal and temporo-parietal activation (LpOp, PT and TPJ in Table 2 and Fig. 3) that is involved when auditory inputs need to be segmented in a meaningful way. Second, the involvement of left inferior frontal and temporo-parietal activation during auditory segmentation tasks might be a consequence of auditory short-term memory, covert articulation or vocalisation mechanisms. Third, the left planum temporale (PT in Table 2 and Fig. 3) on the dorsal surface of the superior temporal gyrus is activated by imagining sounds (in silence) as well as hearing sounds. This suggests that the left planum temporale might be the recipient of top-down processing from higher-order language areas.

30Speech sound processing refers to the unique dynamic acoustic patterns that can be generated by the human speech production system. Abstract knowledge of familiar speech sounds is referred to as phonological memory and can be accessed from visual stimuli (e.g. text) as well as auditory speech. Although there was an expectation that there would be brain areas that were dedicated to auditory speech processing, none of the areas discussed below turned out to be uniquely activated by speech.

31Two studies investigated speech processing during decisions on the sound structure of speech relative to nonspeech sounds (e.g. tones) and reported speech-related activation in bilateral secondary auditory cortices and the left posterior inferior frontal cortex. The interpretation of this speech related activation was in terms of pre-lexical processing in the bilateral secondary auditory cortices with articulatory recoding (i.e. subvocal articulation of the speech sounds) in the left posterior inferior frontal cortex. However, the comparison of speech and tones in these early studies did not control for auditory complexity or auditory segmentation and, as described in the Auditory processing that is common to speech and nonspeech sounds section above, activation in the bilateral auditory cortices and the left posterior inferior frontal cortex was not specific to speech.

32It was also demonstrated that activation for speech depended on task. For example, passive listening tasks were associated with left lateralized activation for words relative to tones in the superior temporal sulcus, middle temporal gyrus and angular gyrus, with inferior frontal activation that was more ventral and anterior to that observed during phonetic judgements and auditory repetition (BA 45 vs. BA 44; ). The same ventral inferior frontal areas were subsequently associated with semantic analysis (see Speech comprehension section below) which is not controlled during the passive listening tasks.

33Consideration was also given to the importance of the ventral part of the left anterior supramarginal gyrus (vSMG) in speech processing. One interpretation was that co-activation in this area and the left posterior inferior frontal cortex was related to articulatory rehearsal during auditory short-term memory tasks and phonological decisions. The alternative interpretation was that ventral supramarginal gyrus activation was related to stimulus encoding rather than memory mechanisms.

34The special role of the left posterior temporal lobe in speech processing was re-considered. reported a common response to speech and nonspeech stimuli in the upper surface of the gyrus but identified a more ventral region in the left lateral posterior superior temporal sulcus (pSTS in Fig. 3) that was activated by both word perception and the retrieval of words from memory (in response to a semantic cue). therefore proposed that this area is involved in transiently representing the temporally ordered sound structure of both heard words and words retrieved from lexical memory. This function would serve a number of key language tasks such as mimicry, repetition and the long-term acquisition of new words. The key difference between this memory function in pSTS (which is in the sulcus on the lower surface of the superior temporal gyrus) and the posterior planum temporale (which is on the dorsal surface of the superior temporal gyrus) is that pSTS is more involved in speech than nonspeech whereas the planum temporale does not distinguish speech and non-speech (see Auditory processing that is common to speech and nonspeech sounds section).

35The speech selective auditory response in the left posterior superior temporal sulcus was repeatedly demonstrated even when acoustic complexity was controlled. Further evidence that these speech selective responses relate to familiarity with the patterns of spectral variation came from two studies that showed activation in the left posterior temporal gyrus/sulcus increased when sine wave analogues of speech were recognised as speech relative to when the same stimuli were not recognised as speech. A contrasting pattern of response was observed in the anterior processing stream where activation was typically observed when acoustic complexity was not controlled, even when familiarity and conceptual content were matched by comparing speech to familiar environmental sounds. Together, these studies are consistent with the previous claims that the posterior superior temporal cortex is related to sound familiarity while the anterior superior temporal gyrus is related to the acoustic complexity of speech.

36Critically, speech selective responses (more activated for speech than nonspeech sounds) do not imply “speech specificity” because both the anterior and posterior temporal speech areas each respond to nonspeech stimuli (e.g. environmental sounds, pitch changes, melodies, familiarity or conceptual processes). It therefore became apparent that specialisation for speech is not localized in dedicated brain areas but is characterised by a distributed pattern of activity across many different areas that are each involved in speech and nonspeech processing, depending on the type of task.

37In the left inferior frontal areas that were activated during auditory categorisation tasks (Auditory processing that is common to speech and nonspeech sounds section) and phonological discrimination tasks, there were increased efforts to dissociate different levels of processing such as selecting, segmenting and comparing. Consistent with previous reports, (i) posterior inferior frontal activation (BA 44) was associated with articulatory recoding or decision mechanisms; (ii) the left ventral premotor cortex was also associated with articulatory recoding when participants passively listened to unfamiliar speech sounds; (iii) ventro-lateral prefrontal cortex was associated with working memory demands and (iv) the mid-dorsolateral prefrontal cortex was associated with stimulus monitoring. Altogether, there was a growing perspective that inferior frontal or premotor activations during auditory speech processing were the consequence of top-down supplementary mechanisms that constrain bottom up speech processing in temporal regions, particularly when speech is unfamiliar or ambiguous. In addition, there were reports that the left inferior frontal cortex was activated when observing nonverbal actions with the suggestion that it might be involved in the interpretation of movements in general rather than being specific to articulation.

38As shown previously, activation for auditory speech processing was primarily left lateralized when other factors were controlled, the speech selective response in the left anterior superior temporal cortex was related to the acoustic content of the stimulus; and the speech selective response in the left posterior superior temporal cortex was related to (a) the familiarity of auditory spectral patterns, (b) the maintenance phase of phonological working memory and (c) the perception of hearing speech.

39Activation in the left premotor cortex during speech processing was associated with better perceptual performance, particularly when the acoustic input was sparse. However, as premotor activation was not found to be sensitive to articulatory complexity during speech perception, suggested that motor representations were incompletely activated during perception. The premotor response during perception was also found for non‐speech sounds. This implies that either the premotor response was not involved in articulation or that subarticulatory activation occurs during the perception of non-speech sounds.

40In the left posterior part of the inferior frontal gyrus and inferior parietal regions, activation was associated with processing syllable order or discriminating sounds on the basis of subtle temporal acoustic features that are typical of phoneme categories. This might be explained by prior association of these areas with auditory short-term memory. There was continued support for the view that the left posterior inferior frontal activation is related to articulatory processes because it was positively correlated with the phonotactic frequency (the pronounceability of combinations of phonemes) of heard sounds. Less support was provided for the prior association of the left ventral anterior supramarginal gyrus with a phonological store because the fronto-parietal verbal short-term memory areas are also activated for unexpected auditory change during tasks that have minimal working memory demands. This suggested that left fronto-parietal responses during speech may be related to nonverbazl auditory attention and categorization functions that provide top-down regulation of auditory functions.

41Depending on the task, left lateralized activation for speech relative to acoustically matched nonspeech sounds was reported in: (1) the left posterior superior temporal cortex (pSTS in Table 2 and Fig. 3) where it was consistently related to sound familiarity; (2) the left anterior superior temporal gyrus (aSTS in Table 2 and Fig. 3) where it was consistently related to the acoustic complexity of speech; (3) the left inferior frontal and premotor areas (LpOp and vPM in Table 2 and Fig. 3) where it was consistently related to articulatory re-coding that places top-down constraints on the disambiguation of speech sounds; and (4) the ventral supramarginal gyrus (vSMG in Table 2 and Fig. 3) where there is accumulating evidence of involvement in auditory attention and categorization functions that that are not specific to speech.

42Overall, the results suggest that phonological processing of speech sounds arises from the functional integration of acoustic processing (in temporal lobe regions) and articulatory processing (in premotor and frontoparietal regions). This is consistent with the growing appreciation that speech processing areas are activated by non-speech stimuli and that functional specialisation arises in the network of regions that are activated. Another important step forward was to consider how different parts of the network parcellated into different processing streams and how these streams are supported by anatomy and functional connectivity.

43Speech comprehension occurs when familiar sounds are recognised and mapped onto their meanings. Many cognitive processes are involved. For example, short-term auditory memory is required because speech is a serial dynamic auditory signal that needs to be integrated over time, particularly when multiple words are presented in a sentence. Accessing meaning also requires selection from multiple competing representations of speech sounds that may sound very similar (sun, some) or the same (sun, son), but have different meanings that are determined by the context. Given the complexity of the processes involved, an early distinction was made between semantic representations and task dependent “strategic/executive/control” processes that are required to access, retrieve, compare and manipulate semantic knowledge.

44A direct comparison of semantic decisions on auditory words to phonological decisions on nonwords demonstrated widely distributed activation in the left middle and inferior temporal gyri, left superior frontal cortex and bilateral angular gyri. These early Demonet et al. studies also played an important role in dissociating (a) temporal lobe regions involved in pre-lexical processing (bilateral superior temporal gyri) from temporal lobe regions involved in semantic processing (left middle and inferior temporal gyri); and (b) parietal lobe regions involved in phonological decision strategies (supramarginal gyri) from parietal lobe regions involved in semantic processing (angular gyri). Subsequently, the role of the left middle and inferior temporal gyri and left angular gyrus was also reported for semantic decisions on written words and pictures. This highlighted an amodal semantic system that was common to auditory words, written words and (nonverbal) pictures. Together these studies suggested that semantic decisions on the meaning of words involve the left middle and inferior temporal and angular gyri while phonological decisions on the sound content of words involve the supramarginal gyri and the left posterior inferior frontal gyrus.

45At the narrative level, demonstrated that listening to meaningful stories, relative to unmeaningful speech, increased activation in bilateral temporal poles and demonstrated that comprehension of sentences (compared to a lexical-decision task) induced extensive activation in several regions of the left hemisphere, including the prefrontal and basal frontal cortices, the middle and inferior temporal gyri and temporal pole, the parietal cortex and the precuneus. In addition, when the sentences had metaphorical meanings, there was right hemisphere activation in the prefrontal cortex and middle temporal gyrus and posterior cingulate. Within this widely distributed system, activation could relate to many different levels of processing such as auditory short-term memory, grammatical deconstruction or semantic processing. Although the studies in this era were not able to interpret the contribution of each of the areas reported, the results showed that language comprehension involves widespread distributed systems in both left and right hemispheres. This pushes us way beyond the appealing simplicity of the early neurological model.

46The involvement of widely distributed temporal, parietal and frontal brain areas in speech comprehension continued to be reported. These effects are more likely to reflect amodal semantic processing than access to semantics from speech sounds because they were commonly activated irrespective of whether the stimuli were auditory or visual words. When access to semantic associations was made more challenging, activation in the prefrontal and angular gyri increased: for example, when speech complexity increased, when reading sentences with semantic violations or when listening to a non-native language.

47There was continued emphasis on the importance of Broca's area (BA 44 and sometimes BA 45) for syntactic processing even when articulation was suppressed. Although the same frontal lobe regions were activated by semantic processing, morphologically complex words and lexical decisions on verbs relative to nouns, a striking double dissociation was observed with greater activation in the left dorsal pars opercularis for syntactic than semantic processing and greater activation for semantics than syntactics in the ventral inferior frontal gyrus (BA 47, pars orbitalis; ) or the right inferior frontal lobe. However, other studies did not show such a clear cut dissociation between semantic and syntactic processing.

48The importance of the auditory processing pathways that projected anteriorly from Heschl's gyrus was highlighted by who identified a region in the left anterior superior temporal sulcus (aSTS) that was activated by intelligible speech when all other characteristics of speech were controlled. Greater aSTS activation was also reported for words relative to syllables and auditory sentence processing relative to environmental sounds, with activation extending into the left temporal pole for higher-level discourse processing. Other areas associated with speech comprehension included the left medial temporal cortex and right temporal and frontal regions, although the contribution of each area remained unclear.

49The substantial overlap in the areas involved in speech comprehension as well as production was reported by and. For example, reported activation common to both listening to stories and verb generation in the pars opercularis and triangularis of the inferior frontal gyrus (Broca's area), the posterior part of the superior temporal cortex centred around the superior temporal sulcus (Wernicke's area) but extending into the posterior part of the planum temporale and the most anterior part of the left inferior temporal gyrus at the junction with the anterior fusiform gyrus (the basal temporal language area) and the inferior and lateral parts of the right cerebellar cortex. This overlap is likely to reflect the many processes that are common to speech production and comprehension, for example, semantic processing, articulatory planning and short term memory. A review of neuroimaging studies of semantic processing in this time era can be found in.

50New areas associated with syntactic processing during comprehension were the right inferior frontal regions, the left caudate nucleus, insula, planum polare bilaterally and the superior frontal cortex. Reviews of syntactic processing at this time can be found in and.

51When accessing semantics from speech sounds, activation was reported to extend from the superior temporal gyri ventrally into the left middle temporal cortex (BA 21; ); dorsally and posteriorly into the left posterior temporoparietal cortex and anteriorly into the ventral anterior temporal cortex (BA 38; ). When the demands on semantic retrieval increased, activation was also observed in the ventral inferior frontal cortex, the left fusiform gyrus, and the angular gyri. All these areas were commonly activated during comprehension of spoken and written language. They are therefore not specific for accessing semantics from auditory speech.

52Within the amodal semantic system, the left anterior temporal pole was particularly involved in specific semantic representations and for meaningful relative to meaningless sentences. The ventral inferior frontal cortex was associated with strategic semantic processing, more dorsal posterior frontal areas were associated with attention demanding speech comprehension tasks and the left superior frontal gyrus was activated when a word's meaning depended on semantic context.

53The influence of grammatical analysis or morpho-phonological segmentation on inferior frontal activation continued to be emphasized, with claims that the left prefrontal cortex is more specialised for syntactic processing during sentence comprehension than other domain-general processes such as short-term memory. Likewise, the role of the basal ganglia in syntactic processing continued to be of interest with proposing that, while inferior frontal and anterior temporal cortices were involved in early syntactic processing, the basal ganglia were involved in late syntactic processing. Other studies emphasized that sentence comprehension is a complex task that involves both language-specific processing components and general cognitive resources that recruit the anterior cingulate, premotor cortex and prefrontal lobe regions regardless of syntactic complexity.

54As shown previously, increasing attention to the meaning of speech involves left lateralized activation extending anteriorly, laterally, ventrally and posteriorly from Heschl's gyri in multiple different pathways. In the temporal lobe, activation extended into the anterior and posterior areas in the middle temporal gyrus, posterior inferior temporal gyrus, anterior fusiform and the hippocampus (in medial temporal cortex). In the parietal lobe, semantic activation was reported in the posterior temporoparietal cortex, the left angular gyrus and precuneus. In the frontal lobe, semantic activation was reported in the left pars orbitalis and middle and superior frontal gyri. These areas were again reported for semantic processing of written words and pictures of objects, consistent with their role in amodal conceptual processing or semantic control.

55The emphasis on left lateralized activation does not exclude the contribution of the right hemisphere homologue areas which were shown to be particularly involved during tasks that required executive processing and/or the integration or consolidation of semantic concepts, for example, when the words “boat” and “house” occur together, they refer to a single concept meaning “a shelter for boats”.

56The functional role of each semantic area unravelled further, with the involvement of each area depending on the task demands and the baseline condition. Anterior temporal activation was linked to semantic associations because it was observed during passive listening, except when the baseline task was at rest which was argued to inadvertently control for semantic processing because free flowing thought is richly semantic in nature. Posterior middle temporal activation was more sensitive to semantic demands because, although it was observed during passive listening, activation increased with executive demands and when semantic information was received in both auditory and visual modalities simultaneously. Activation in ventral frontal regions in the left pars triangularis/orbitalis also increased with the executive demands of the task, for example during conditions where competition from semantically similar targets was high versus low. This is consistent with a role in selection and retrieval of semantic representations. Parietal activation in the angular gyrus and retrosplenial/posterior cingulate was not typically observed during passive listening but was observed during lexical decisions on words compared to pseudowords, during memory demanding comprehension of narratives. The left medial parietal cortices (precuneus and posterior cingulate) were associated with updating story representations in narrative language comprehension. In contrast, the angular gyri were associated with integrating and retrieving concepts and top-down predictions of semantic content. It also became apparent that there were several different functionally distinct subregions in the angular gyrus. For more comprehensive reviews of the semantic system, see and.

57Dorsal frontal regions in the left premotor cortex and pars opercularis were more activated when sentence meaning was ambiguous or implausible relative to plausible (; Ye et al., 2009; ). Explanations for why activation in these areas is greater for implausible sentences include the following: (a) activation in the left premotor cortex reflects covert articulatory processing; (b) activation in the ventral pars operculum reflects articulatory planning and verbal working memory; (c) activation in the left dorsal pars opercularis reflects linguistic and non-linguistic sequencing, decision making and top-down processing that attempts to predict the most likely meaning or sound while (d) activation in the right pars opercularis reflects conflicting semantic information and nonlinguistic executive and attentional processing. A 20 year review of semantics and syntax can be found in.

58Many left lateralized areas are involved in accessing semantics from auditory speech and other stimuli. Anterior temporal areas (aSTS, LaMTG/LaITG in Table 2 and Fig. 3) are involved in accessing increasingly specific semantic associations, with activation for sentences and narratives spreading anteriorly into the temporal pole. Posterior temporal areas (pMTG, pITG in Table 2 and Fig. 3) are increasingly involved as the semantic content or task demands increase. Ventral inferior frontal areas (pOrb and pTri in Table 2 and Fig. 3) are involved in selecting and retrieving task related semantic attributes. The dorsal superior frontal gyrus (SFG in Table 2 and Fig. 3) is also involved, albeit less consistently, in constraining semantic processing. The angular gyri (ANG in Table 2 and Fig. 3) have been associated with the crossmodal integration of semantic features and in predicting the semantic nature of the stimulus while more medial parietal areas (precuneus and posterior cingulate) are more involved for narrative than single word comprehension. The above descriptions of the functional role of each region are clearly vague and insufficient. The anatomical localization of the anatomical regions is also insufficiently precise. We are therefore far from understanding how the human brain supports speech comprehension.

59The processing involved in speech production overlaps with that involved in speech comprehension. For example, both involve access to the semantic system. In addition, subarticulatory processing may be automatically involved in discriminating auditory words while auditory imagery may be automatically involved in articulation. This section focuses on those processes that are more involved in production than comprehension. There are no separate sections for word and sentence production because these have been shown to involve the same neural structures.

60The left prefrontal activation associated with word generation included dorsal and ventral inferior frontal areas (BA 44, BA 45, BA 47) and medial frontal areas. The middle frontal cortex (BA 46) and medial frontopolar prefrontal cortex (BA 10) were related to semantically driven word retrieval because they were more activated during verb generation (generate “eat” in response to “cake”) relative to phonologically constrained stem completion (generate “green” in response to “GRE”). In contrast, the posterior inferior frontal regions (near BA 44 or BA 45) were activated during stem completion as well as verb generation suggesting a less semantically determined role in word retrieval. With practice, activation in all these prefrontal areas decreased while it increased in the bilateral sylvian-insular cortex, as predicted by prior claims that the insula was more involved in automatic speech production than word retrieval (Mohr, 1978).

61The temporal lobe areas associated with word retrieval tasks included: the left temporoparietal cortex, left posterior superior temporal gyrus, left posterior inferolateral temporal cortex and bilateral superior temporal gyri. The left posterior temporoparietal cortex and the left inferolateral temporal cortex were more involved in producing words than listening to words, the left posterior superior temporal gyrus was commonly activated during speech production and perception and activation in the bilateral superior temporal gyri during overt speech production was attributed to auditory processing of the participants ‘own voice’ because the same regions were also activated when listening to ‘another's voice' from a pre-recorded tape, see Auditory‐motor feedback during speech production section below.

62The left anterior frontal areas (middle frontal/BA 46 and pars triangularis/BA 45) were consistently reported during the most demanding word retrieval tasks such as verbal fluency, sentence generation and some picture naming paradigms, but not other plausibly easier picture naming tasks. Functionally, these prefrontal activations were associated with: (i) semantic working memory regardless of stimulus modality, (ii) the selection of words from many competing alternatives, and (iii) response suppression.

63The anterior cingulate was also associated with response suppression during verbal fluency tasks. For example, found that the anterior cingulate cortex was activated during a verb-generation task when there was competition among alternative responses. This functional account of anterior cingulate activation explains the higher response in this area during sentence completion than reading aloud because multiple meanings are generated in the course of producing an appropriate completion. also showed that the part of the anterior cingulate that was relevant to word generation was a posterior dorsal subregion that is anatomically connected to lateral motor systems.

64In the left posterior inferior temporal lobe, activation was again reported during semantically mediated word retrieval tasks such as picture naming and sentence generation but the more medial aspect of this area, in the vicinity of the occipitotemporal sulcus, was also observed for the retrieval of colour and letter names that place minimal demands on semantics. The association of this posterior inferior temporal region with word retrieval in the absence of visual or auditory stimuli was unexpected but consistent with observations that damage to the posterior inferior temporal cortex causes anomia and electrical stimulation to the inferior temporal cortex caused receptive and expressive language difficulties. It was nevertheless clear that there are multiple posterior inferior temporal areas involved in word retrieval including: (i) a lateral posterior inferior temporal region involved in generating verbs and nouns from heard words; (ii) the anterior fusiform gyrus that was commonly activated for word retrieval and comprehension but more activated for semantic than phonological decisions; and (iii) more posterior inferior temporal/occipitotemporal regions that are more involved in naming than viewing pictures, words, letters or colours.

65In the left posterior superior temporal cortex, and replicated the study by showing activation for word repetition when sensorimotor activation is controlled. advanced this finding by showing that it was the most posterior and medial part of the planum temporale, at the junction with the inferior parietal lobe (i.e. the temporo-parietal junction), which was more activated by speech production than speech perception, even though this region was consistently associated with auditory speech processing that did not involve speech production (See Auditory processing that is common to speech and nonspeech sounds and Speech selective auditory responses).

66In an extended review of studies published up until 2001, associated: (a) the mid part of the left middle temporal gyrus with semantically driven selection of a lexical item because it was commonly activated by word generation and picture naming but not by word reading; (b) the posterior middle and superior temporal gyri with lexical word form retrieval from a phonological store because it was commonly activated by picture naming, word generation, and word reading, but not pseudoword reading and (c) frontal lobe areas with later stages of speech production such as articulatory planning (see Covert articulatory planning section for rationale).

67There was a relative paucity of speech production studies published in this time era because fMRI scanners had largely replaced PET scanners and investigators were concerned about the potential interference from head motion on BOLD signal during speech production. Nevertheless, the brain areas associated with word retrieval in previous years were largely replicated with refined function and further anatomical dissociations. This resulted in a clearer appreciation that word retrieval involved: (a) the anterior rather than the posterior left prefrontal cortex (BA 45/46 versus BA 44; ); and (b) lobules VI and VIIB in the right posterior lateral cerebellum in those with left lateralized frontal activation or the left homologues of these areas in those with right lateralized frontal activation.

68In the right pars opercularis (BA 44), activation was found to be reduced for the generation of narrative (propositional) speech compared to a baseline nonspeech condition with no right frontal activation for generating words relative to generating nonsense syllables. hypothesized that the right basal ganglia (caudate nucleus and putamen) suppressed right frontal activation to reduce interference during language and this resulted in left lateralized activation in the inferior frontal, pre-SMA, thalamus and basal ganglia regions. However, others found that right prefrontal activation increased when word selection became more difficult, for example when the constraints on word selection were reduced or during the generation of narratives. As there are several different frontal regions being referred to, in two different hemispheres, and under various tasks, the determinants of right frontal activation remained unclear.

69As shown previously, word retrieval was strongly associated with activation in the left anterior prefrontal cortex including BA 45 in the left inferior frontal cortex and BA 46 in the left middle frontal gyrus, even when articulation and conceptual processing were controlled and this was accompanied by activation in the right vermal and hemispheric components of lobule VI and Crus I and II of lobule VII in the posterior lateral cerebellum. Right frontal activation was more likely to be observed in the context of more retrieval effort which may explain the corresponding increases during paced relative to unpaced word production and for older relative to younger participants. Within the anterior cingulate, an anterior zone was associated with conflict monitoring (response suppression) which might be more related to word retrieval than the posterior zone associated with general response selection.

70When word retrieval became more semantically demanding, for example when subjects were instructed to retrieve narratives or when distracting semantic information was added, activation for word retrieval was also reported in the medial superior frontal cortex, the left pars orbitalis in the ventral inferior frontal cortex, the left angular gyrus/inferior parietal cortex, left ventrolateral temporal cortex and the left hippocampus. However, these anatomically distributed brain areas are likely to reflect silent conceptual processing (see Speech comprehension section) rather than word retrieval per se.

71When word retrieval became more demanding, in the context of minimal semantic constraints, activation was reported at the left temporoparietal junction, for example, when producing picture names with low relative to high word frequency, for words which lack a phonological neighbour and in the presence of phonological relative to semantic interference. As the same temporoparietal area was activated when the post-articulatory auditory feedback was altered to create a conflict between the expected auditory response to the spoken name and the actual auditory response, the increased temporoparietal activation during challenging word retrieval tasks may simply be a consequence of increased verbal self-monitoring during which the word produced is compared with the intended output; see Auditory‐motor feedback during speech production section on post articulatory auditory motor feedback below for further discussion.

72The most consistent activation for word retrieval from semantics when articulation and semantics are controlled were: the left middle frontal gyrus (MFG in Table 2 and Fig. 3), Crux 1 of the right lateral (l) posterior (p) cerebellum (CB) and posterior regions in the left middle and inferior temporal cortices (L.pMTG and LpITG in Table 2 and Fig. 3), with more dorsal superior temporal lobe regions (pSTG and TP in Table 2 and Fig. 3) when retrieval becomes more difficult and an anterior zone in the anterior cingulate (ACC a zone in Table 2 and Fig. 3) associated with response suppression.

73Premotor stages of speech production can be investigated with covert articulation tasks that involve the silent production of speech sounds without movements in the articulators or phonation. In addition to motor planning, this level of processing can evoke “inner speech” because the auditory images of speech can be heard in our heads when we prepare to articulate words even though there is no auditory stimulation.

74During silent articulation and verbal working memory, activation in the left posterior inferior frontal gyrus (Broca's area, BA 44) and/or left premotor cortex (BA 6) was associated with “inner speech”. This was consistent with the view that the left posterior inferior frontal gyrus was involved in auditory-articulatory mapping which resulted in subvocal articulation during perception and auditory imagery of speech during articulation.

75Covert articulation was again associated with activation in the left posterior inferior frontal region (pars opercularis, BA 44) because this area was activated during: silent word generation, subvocal rehearsal of phonological information, silent syllable counting when presented with written pseudowords, segmentation of speech sounds and by letter relative to semantic fluency. There were two unexpected observations. The first was that there was surprisingly little posterior inferior frontal activation during auditory word repetition and reading aloud with no significant activation difference between word or pseudoword repetition but consistently higher activation for reading pseudowords than words. This suggests that left posterior inferior frontal activation was less in the context of phonological cues and more when the articulatory associations of the word were unknown or needed to be held in short term memory. The second unexpected observation was that it became increasingly apparent that activation in Broca's area was not specific to speech. For example, reported left lateralized posterior inferior frontal activation for imagining a moving target and suggested that it was involved in mediating higher-order movement control of forelimbs as well as speech. This observation indicates that the left posterior inferior frontal cortex is more involved in motor planning than in auditory imagery or inner speech.

76The contribution of the left anterior insula to articulatory planning was suggested in both functional imaging and lesion studies. This explained why the left anterior insula was activated during a range of tasks including overt picture naming. Greater left anterior insula activation for overt than covert articulation also suggested that the left insula might be more directly involved in the coordination of the various (up to 100) muscles engaged in articulation and phonation.

77Activation in the SMA and bilateral anterior cerebellum (lobules IV and V) during silent articulation tasks suggested that the contribution of these regions to other tasks such as overt picture naming, vocalisation and breathing occurred prior to vocalisation. A role for the SMA in the timing of speech and nonspeech motor commands was suggested following observations that the SMA was activated during silent articulation and memory-timed finger movements. In contrast, proposed that cerebellar activation during silent articulation was the consequence of subliminal activity of orofacial and laryngeal muscles.

78The opercular part of the posterior inferior frontal cortex (pars opercularis, Broca's area, BA 44) was associated with forming or dividing words into syllables (syllabification) during both covert (silent speech) and overt (speaking aloud) production or translating speech into articulatory code. Within the pars opercularis, a distinction was made between dorsal and ventral parts with the dorsal part activated by action observation as well as imitation but the ventral part activated by imitation more than observation. This suggests that the ventral pars opercularis has a more motoric function than the dorsal pars opercularis.

79More posteriorly, in the left premotor cortex (BA 6), activation was associated with compiling motor codes for syllables and a “speech sound map” that linked phonemes or frequent syllables to their associated motor programs. Although different parts of the dorsal pars opercularis and premotor cortex were found to be responsive to the observation of hand, mouth and foot movements, no speech specific areas were identified when speech was compared to nonspeech motor functions. For example, the dorsal pars opercularis was associated with sequencing the motor acts required to produce hummed notes as well syllables.

80A rostrocaudal gradient distinction was made between the pre-SMA and the more posterior SMA-proper: During silent articulation, the pre-SMA was associated with sequencing abstract motor plans while the SMA-proper was associated with the control of motor output. This distinction was supported by observations that the SMA was commonly activated by word generation and reading when articulation was matched but the pre-SMA was more activated by: (a) word generation than reading,, (b) during the covert rather than overt stage of object and action naming, and (c) pseudoword repetition when the phonological complexity of the stimulus increased.

81In the left pars opercularis (Broca's area/BA 44), a clearer distinction emerged to dissociate the function of the ventral and dorsal parts. The ventral left pars opercularis was activated during covert articulation with increased activation for phonological relative to semantic retrieval, consistent with a role in articulatory recoding of speech. The left dorsal pars opercularis was associated with processing prior to articulatory recoding and was found to be commonly activated by both the production and observation of nonsemantic, nonsyntactic, and nonsense syllables. The dorsal premotor cortex was associated with general action selection because it was observed during finger movements as well as speech while the left ventral premotor cortex was associated with generating the motor acts related to speech sounds, nonspeech sounds and orofacial movements such as tongue protrusion and lip pursing that are not associated with sound production.

82In the pre-SMA, activation was associated with inhibiting rather than initiating vocal and manual responses. The inhibitory role for the pre-SMA may explain why activation was found to be greater for volitional relative to stimulus driven mouth movements because selecting the correct response (in volitional mouth movements) requires competing responses to be inhibited. It may also explain the numerous reports that pre-SMA activation is greater for the production of unfamiliar speech sounds in terms of the increased effort in suppressing prepotent familiar speech.

83Finally, evidence that activation in the anterior insula, subcortical structures (basal ganglia and thalamus), cerebellum, planum temporale and inferior parietal lobe was reduced during the silent short-term maintenance of auditory stimuli when articulation is suppressed, suggests that these areas are more involved in articulatory activity. Conversely, it was also noted that activation in the planum temporale and inferior parietal lobe was higher during covert than overt production of sentences and during covert (imagined) than overt singing. This suggests that activation in these temporo-parietal regions might be related to the sensorimotor circuits that maintain sound representations for the production of speech and song.

84Covert articulation is a mix of processing that occurs prior to overt articulation and independently from word retrieval. The mapping of heard or intended speech to orofacial movements has been associated with activation in the ventral pars opercularis (pOpv in Table 2 and Fig. 3) and the ventral premotor cortex (vPM in Table 2 and Fig. 3) with subliminal motor activity in lobules IV and V of the bilateral anterior medial cerebellum (a CB). In contrast, mapping in the reverse direction (from orofacial movements to auditory imagery) involves the auditory imagery areas discussed in Auditory processing that is common to speech and nonspeech sounds section (i.e. PT and vSMG in Table 2 and Fig. 3). Covert articulation also activates areas that are engaged by other motor modalities (e.g. fingers), for example, the left dorsal pars opercularis (LpOp-d in Table 2 and Fig. 3) associated with motor sequencing; and the bilateral premotor cortex (d-PreC in Fig. 3).

85This section considers the brain areas that control mouth movements (lips, tongue, jaw), the vocal tract (larynx) and breathing during overt speech production.

86When syllables were articulated without using the larynx, activation increased in the left primary motor cortex that controls the face, the upper pons, the left planum temporale and the left posterior perisylvian cortex. The response in auditory regions (left planum temporale and left posterior perisylvian cortex) was observed even when auditory processing of the spoken response had been minimised and masked out using low-intensity white noise. This was explained in terms of motor activity (left motor primary cortex) causing a discharge corollary of the motor command to sensory structures.

87Tongue movements were found to produce symmetrical activation at the lower primary motor cortex, with left lateralization in the same region during automatic speech and right-sided activation during singing. There was, nevertheless, a striking overlap between the areas activated during the articulation of speech, vocalisation and the control of volitional breathing in the absence of vocalisation. For example, controlled breathing activated dorsal primary motor cortices bilaterally, the lateral pre-motor cortex in the right hemisphere, the SMA and left ventrolateral thalamus, with additional activation for expiration in more bilateral ventrolateral primary motor areas. This emphasizes that the motor and premotor activation during speech involves far more than simply moving the mouth.

88Investigation of the role of the anterior cingulate cortex in higher-order motor control showed that speech activated the intermediate dorsal and the rostral ACC which is distinct from more anterior regions involved in the control of manual tasks. The authors proposed that the anterior cingulate participates in motor control by facilitating the execution of the appropriate responses and/or suppressing the execution of the inappropriate ones.

89The role of the left putamen in speech production was also discussed in a paper by who observed that left putamen activation was higher for auditory repetition of words in a non-native language than the native language which can be explained in terms of increased demands on the articulatory system.

90The control of the tongue was localized in the central sulcus (BA 3/4) at approximately 28 mm above the intercommissural plane. Contrary to previous findings, activation was observed bilaterally rather than being left lateralized. also identified bilateral premotor areas during tongue movements and segregated these effects from the primary motor and sensory cortex activations for lip movements. Of more relevance for speech, found that the activation for articulating the syllables “pa” and “ta” corresponded to activation related to nonspeech lip and tongue movements respectively.

91The control of breathing was investigated by who found bilateral sensorimotor and motor cortex activation that was medial to that associated with the articulators. The same study showed that the thalamus was activated during the control of breathing as well as articulation and this may explain some of the left lateralized thalamic activation observed during verbal fluency, naming objects, naming letters, naming colours and reading especially when the rate of speech production increased. Activation was also left lateralized in the putamen during an overt versus silent stem completion task and in the posterior pallidum during auditory repetition. However, while activation in the motor cortex and left thalamus increased with the rate of speech production, activation in the left putamen was higher for slower production rates. These findings emphasized the importance of left lateralized subcortical responses during speech production and dissociated the function of the left thalamus (associated with breathing) from that in the basal ganglia (associated with the timing of production).

92A direct comparison of overt speech production with motor preparation activated regions in the primary motor and somatosensory cortices, SMA, insula, thalamus, basal ganglia and posterior cerebellum. The association of the left insula with motor processing rather than articulatory planning was emphasized again following observations that left anterior insula activation was higher for overt than covert speech and unaffected by the demands on motor planning. Left lateralized activation during overt articulation was observed in the insula and the dorsolateral premotor cortex and this was contrasted to the bilateral activation in sensorimotor cortex. Similarly, left lateralized activation in the primary motor cortex for phonation was contrasted to bilateral activation for tongue movements.

93The motor function of the SMA-proper was re-iterated and associated with the voluntary control of learnt motor sequences of both speech and finger movements. This is not incompatible with the involvement of the SMA in the motor control of breathing (see Overt articulation Time era: 1992‐1996 section) which needs to be finely timed with the mouth movements producing sounds. In the cerebellum, the areas activated by speech articulation were in the left and right medial superior posterior cerebellum (paravermal lobule VI) and these areas were separated from the right lateral superior posterior cerebellum (HVI/Crus I) associated with word generation and the right inferior posterior cerebellum (HVIIIA) that was activated by vocalisation and breathing during articulation and during passive listening to auditory clicks that varied in frequency. A distinction was also made between activation for articulation in the left and right medial posterior cerebellum and the striatum (caudate and putamen) because increased rate of articulation had a positive influence on activation in the cerebellar regions and thalamus but a negative influence on activation in the striatum. Thus, the putamen and caudate were more activated for slower (more controlled) speech production. This might explain why left putamen activation was associated with counting and reading written syllables and is consistent with prior claims that the putamen is involved in the timing of speech production.

94All the above areas (left anterior insula, bilateral premotor and sensorimotor cortices, posterior cerebellum, SMA, thalamus and striatum) were activated for producing melodies and whistling as well as speech. This is consistent with specialisation for speech production emerging from the co-ordination of the language system (semantic processing, word retrieval and the sequencing of this information) with mouth movements, vocal tract movements and breathing.

95As shown previously, the areas that are activated by speech were also activated by nonspeech orofacial movements and vocal tract gestures, sniffing, singing, volitional exhalation and phonation. The contribution of phonation to activation in the bilateral sensorimotor cortex during articulation was also emphasized in several studies. identified a larynx-specific region in the motor cortex by comparing vocal and nonvocal laryngeal tasks (phonation) relative to vowel, lip movement, and tongue movement. investigated this further describing a dorso-ventral somatotopic organization of lip, jaw, vocal/laryngeal, and tongue movements.

96Activation in the left anterior insula, on the junction of the frontal operculum, was sensitive to the complexity or novelty of subsyllabic verbal utterances. Opinions on the role of the insula during articulation changed again with a new focus on its role in the voluntary control of breathing. This is consistent with observations that bilateral insula regions are involved in phonation for speech, volitional exhalation and syllable singing. A role for the insula in the control of breathing may explain why this area is activated during non-verbal orofacial functions including lip movement, tongue movement and vocalisation because mouth movements interfere with the regular pattern of breathing thereby increasing the demands on the control of breathing. A similar explanation may account for why bilateral insula activation increases during overt picture naming when phonological/articulatory interference increases. However, it is more difficult to explain how the control of breathing explains bilateral insula activation during silent tasks such as silent rehearsal of tone (pitch) and verbal information unless breathing is automatically adapted during subvocal articulation.

97In the SMA-proper, activation was greater for complex articulation than prolonged vowel production or exhalation and maintained during production consistent with a role in execution as well as initiation. In the anterior cingulate, the most posterior zone was associated with motor execution, rather than conflict monitoring or response selection but the anterior zone associated with conflict monitoring was found to be more activated by speech than nonspeech. Other studies also found the anterior cingulate cortex involved in the suppression of inappropriate and unintended speech. Such suppression may be less involved in producing nonspeech sounds because selection and production of nonspeech may be slower with less competition from highly similar motor programs.

98In the bilateral medial superior posterior cerebellum, activation related to articulation was located in lobule VI/Crus I. The cerebellum is thought to have a modulatory role in motor functions (Murdoch et al., 2010) and, during articulation, activity in bilateral superior cerebellar regions may contribute to the timing of consonant–vowel syllable production and the online sequencing of syllables into fast, smooth and rhythmically organized larger utterances. Lobule VI is associated with lip and tongue movements, therefore have proposed that it is involved in instantiating internal models of vocal tract articulation during both speech and singing. This contrasts to the function of the right posterior lateral inferior cerebellum (Lobule VII) that was associated with word retrieval (Word retrieval from semantics. Time era 2002‐2006 and Word retrieval from semantics. Time era: 2007‐2011 sections above); and the very ventral and medial parts of lobule VIIIA that are activated when sensorimotor feedback is disrupted (see Auditory‐motor feedback during speech production. Time era 2007‐2011 section below).

99Finally, the left putamen and thalamus were incorporated into a motor loop that passes activity from the SMA via the putamen to the thalamus and into the motor cortex. This is consistent with the basal ganglia being involved in the innervations of vocal tract muscles. A somewhat different view is that the basal ganglia (putamen and caudate) are involved in the timing, predictive coding and sequencing of events and this can be compensated for by a cerebellar-thalamic-pre-SMA pathway. There are also claims that the insula (rather than the SMA) activates the basal ganglia and cerebellum prior to motor output. These connectivity studies showing the interactions between different regions are intriguing but further investigation is required to tie all sources of evidence together.

100Producing the sounds of speech involves more than sensorimotor activity in the pre- and post-central regions (PrC and PoC in Table 2 and Fig. 3) that control the orofacial muscles. It also involves activation related to laryngeal activity, phonation and the voluntary control of breathing. A distinction has also been made between areas involved in motor execution (e.g. ACC in Table 1) and the cerebellum (CB in Table 2 and Fig. 3) and subcortical areas (PUT in Table 2 and Fig. 3) involved in the timing and control of motor activity.

101Articulation of speech produces sound for the listener that will also be heard by the speaker. During language acquisition, auditory processing of self-produced speech is used to tune motor production so that the produced auditory output matches the intended auditory output. In this sense, auditory feedback is useful for monitoring and correcting speech errors. Once speech is mastered, auditory feedback is less useful and we do not actively attend to the sound of our own voice. We may even inhibit auditory processing of the spoken response. Nevertheless, to anyone who has struggled to speak normally on a telephone line that delays the auditory feedback, it is clear that auditory feedback during speech production is not completely inhibited.

102Auditory processing of self generated speech was inferred from observations that bilateral superior temporal gyri were activated during speaking aloud relative to making the articulatory movements of the same words without generating any sound. There were two qualifications to this observation: (a) superior temporal activation during self-vocalisation was less than that expected when perceiving another's voice and (b) left posterior temporal activation (in the planum temporale and perisylvian cortex) was observed during unvoiced syllable production when auditory processing was masked by low-intensity white noise. To explain the activation in auditory processing areas during silent speech production, emphasized that when we engage in motor activity, a discharge corollary to the motor command is sent from motor to sensory structures. Support for this hypothesis came from observations that the left posterior superior temporal cortex, extending into the left planum temporale, was activated when subjects imagined hearing another person's voice in the absence of any auditory input. Together these results suggested that auditory imagery during articulation resulted in left lateralized posterior temporal activation whereas auditory processing of the heard response after articulation resulted in bilateral superior temporal activation. This implies that left posterior temporal activation occurs prior to bilateral superior temporal activation but, to my knowledge, the differential timing of these responses has still not been tested.

103Processing of self-produced vocalisations in bilateral auditory cortices was shown to be less than that of another's speech unless the speech fed back to the auditory system was altered to make it different from the articulated voice. This suggests that, although auditory processing is normally less during articulation, it increases when the heard sounds are not expected. The response in the left planum temporale was again consistent with auditory imagery because it was observed when silently imagining speech or for recalling (imagining) the auditory relative to visual associations of a picture of a scene.

104As shown previously, bilateral superior temporal activation was found to increase when there was a mismatch between the expected and actual auditory feedback. In the left planum temporale (previously associated with auditory imagery), activation was observed during subvocal articulation or the presentation of visual stimuli that had previously been experienced with auditory activity. For example, activation in the left planum temporale increased during the silence that followed familiar music even when there was no instruction to remember the music, when passively viewing finger tapping on the piano following keyboard training, when producing rhythmic finger sequences that had been learnt with an auditory cue and when imagining heard speech, music or environmental sounds in the absence of sound. These studies are consistent with the prior hypothesis that the left planum temporale is involved in auditory imagery and would explain why activation in the left planum temporale increased with the rate of covert (silent) speech production, if we assume that auditory imagery (or inner speech) occurs automatically during covert speech production.

105Auditory imagery during speech production might play an essential role in predicting the intended speech production, or even providing an internal model to which the auditory feedback should be matched. There then needs to be a process by which the anticipated auditory response is integrated with the actual auditory response. This was addressed by who proposed that there were “error cells” in the posterior superior temporal gyrus and planum temporale that respond when there is a mismatch between the intended/expected speech and the sound of the speech. The error signal is then fed back to the primary motor cortex to adjust the speech output so that it can be closer to that which was intended. Likewise, proposed that there were “error cells” in the parietal (somatosensory) cortex that monitor the tactile and proprioceptive sensations.

106In the bilateral superior temporal gyri associated with auditory processing, further studies showed that activation related to processing the sound of the speaker's own voice was less during the process of producing the speech than when hearing a recording of the spoken response. This suppression of auditory processing was proportional to the quality of the feedback; consequently, superior temporal activation increased when speech was distorted (; Christofells et al., 2011; ) or when auditory feedback was delayed.

107Six new findings emerged. First, in the left posterior planum temporale/temporoparietal area that previous studies had associated with the silent imagination of heard speech, activation was found to increase when speech production was more error prone due to interference or speaking in a second language. This is consistent with the mental imagery of the intended speech playing a role in monitoring speech production when it is error prone. Second, the left pars opercularis and left posterior superior temporal sulcus were reported to be more activated for making silent articulatory speech movements relative to silent nonverbal mouth movements, but the left posterior planum temporale was equally activated by verbal and nonverbal mouth movements. This was interpreted in terms of the higher-order language areas that predict the auditory consequences of articulation. It also distinguishes the functional response in the left posterior planum temporale from that in the left pars opercularis and posterior superior temporal sulcus but does not elucidate the distinct contribution of each of these areas. Third, bilateral superior temporal activation was reported to be negatively correlated to that in the SMA which suggests that the role of the SMA in suppressing auditory feedback should be investigated. Fourth, activation in the right prefrontal cortex and rolandic cortical activity increased with bilateral superior temporal activation during distorted feedback which suggested a role for these areas in modulating subsequent speech output, or in resolving interference. Fifth, the posterior medial dorsal surface of the superior temporal gyri, including the planum temporale, were found to be activated during repetitive (silent) movements of the jaw and tongue as well as during auditory feedback and nonspeech vocal tract movements. This highlighted a role for the posteromedial supratemporal plane in polysensory integration. Sixth, bilateral postcentral gyri were associated with somato-sensory feedback and the consequences of this on compensatory speech motor commands were considered by who found that jaw perturbations during speech increased activation in the left and right ventral motor cortex, inferior frontal cortex and inferior posterior cerebellum (lobule VIII).

108Extrapolating from the findings so far, my speculation is that auditory monitoring of the spoken voice starts with an internal model of the intended speech which is generated in the core language areas (pOp and pSTS in Table 2 and Fig. 3). This results in auditory imagery (in STG and PT in Table 2 and Fig. 3). As the predictions become more precise, activity in the auditory cortices (L&R STG) decreases (with more activation when predictions are less precise).

109Written words access the language system via the visual system. The sensory processing is therefore different from that required for the comprehension and production of auditory speech. The mapping of visual stimuli to articulation is also different from that involved in object naming. For example, words written in alphabetic script are composed of a limited number of visual features (letters) that provide clues to the pronunciation of the whole word. Phonology can therefore be retrieved from novel letter combinations that do not have learnt semantic associations (e.g. THACY). This means that there are infinitely more meaningful words that can be read than objects that can be named. Words can also be combined into sentences and narratives. The review of visual word processing below focuses only on the results of studies that aimed to find brain areas that are more activated by reading than either auditory word processing or visual object naming. The first section (Early visual word form processing. Time era: 1992–1996) focuses on brain areas activated by written words more than other types of stimuli. The second section (Dissociating neural pathways for mapping orthography to phonology) considers brain activation that might differ according to whether orthography is mapped to phonology at the lexical, sublexical or semantic level.

110The early neuroimaging studies of reading suggested a special role for the left extrastriate visual cortex in visual word processing. Although the extrastriate cortex is clearly involved in orthographic (letter) processing, subsequent studies emphasized the importance of three different regions in visual word form processing. The first was the left posterior middle/superior temporal gyrus which was more activated for reading aloud than viewing ‘false fonts’ (non-existent letter-like forms that controlled for visual input) and saying a single word (e.g. “crime” or “range”) to control for speech production. The second was the left angular gyrus that was more activated for viewing words than pictures, and also the site of the “visual word form area” in the classical neurological model of reading. The third was the left ventral occipitotemporal cortex that was more activated by reading the Japanese script Kanji than Kana; and more activated when younger relative to older adults read English words.

111Explanations for the inconsistent localization of visual word form processing focused on the experimental design and emphasized that activation changed with the task, the exposure duration of the stimuli, their rate of presentation and difficulties selecting a suitable baseline task because word-like stimuli automatically access the language system irrespective of the task. In brief, subtle variations in experimental design influenced brain activity during reading tasks and it was therefore premature to associate specific processing functions with individual anatomical areas.

112The involvement of the left occipitotemporal cortex in visual word form processing was not disputed. Meanwhile, reading-related activation in the left extrastriate cortex was attributed to early visual processing and that in the posterior middle temporal and angular gyri was associated with semantic processing.

113The strongest and most influential claim was that the left occipitotemporal cortex housed abstract representations of visual words. This led to the left occipitotemporal cortex being labelled the ‘visual word form area’ (VWFA). Although damage to the left occipitotemporal cortex is known to impair reading, confusion and controversy emerged at the level of functional specialisation and anatomy. At the functional level, the abstract visual word processing claim was challenged by observations that activation for written words (that have abstract visual word form representations) was less than that for stimuli that don't have abstract word representations such as (a) unfamiliar pseudowords or (b) pictures of objects. At the anatomical level, the left occipitotemporal activation associated with reading was located on the medial surface of the inferior temporal gyrus, at the boundary with the fusiform gyrus and at the junction between the occipital and temporal lobes. Hence it was referred to with multiple names: posterior inferior temporal, fusiform, occipitotemporal and the “VWFA”. Different sub-divisions of the left occipitotemporal reading area were also dissociated with different functional attributes leading to a situation where the same activation could be given different anatomical and functional labels.

114Reports of activation during visual word form processing continued to focus solely on the role of the left occipitotemporal cortex which was also referred to as the left mid-fusiform gyrus and visual word form area (VWFA). All studies agreed that this area was consistently activated by visual word processing across languages and orthographies (e.g. ). Activation was also reported to be higher for written words than spoken words, written words than chequerboards or consonants; and to be invariant to the spatial location of the stimuli or the case and font of the letters. The anatomical location of the visual word processing activation was also distinguished from other surrounding areas involved in single letter processing and amodal semantic processing.

115Observations that left occipitotemporal activation was observed for pseudowords with increased activation as letter strings became more word-like led to suggestions that learning to read tuned the receptive properties of the underlying neurons to combinations of letters (such as bigrams and trigrams) that are found within familiar words. However, this perspective did not explain why left occipitotemporal activation was less for (a) words with high relative to low lexical frequency or (b) familiar words than pseudowords. To explain these “lexical familiarity effects”, proposed that the left occipitotemporal cortex was specialised for extracting and storing abstract whole word patterns. According to this account, the amplitude of the activation increases with the difficulty encountered when matching a visual word form to its lexical representation (i.e. low > high frequency words; pseudowords > words). This lexical account can explain why left occipitotemporal activation is reduced by the repetition of a word (“sold–sold”) but not to a repetition to a pseudoword (“solst–solst”) but cannot explain why left ventral occipitotemporal activation was sensitive to sublexical similarities between words (e.g. “corner–corn”) that had different lexical representations.

116A third perspective was that the same left occipitotemporal neurons were activated by object recognition and colour naming tasks and therefore the function of this region was not specific to either letter combinations or whole word forms. Instead, the function appeared to be one that integrated visual information with higher-level processing. This would explain why activation in this region was sensitive to lexicality effects and prior experience. It also explains why the left fusiform responses to letters relative to unfamiliar shapes were task dependent and why left occipitotemporal responses to novel orthographic stimuli changed with the type of training experienced. For example, found that activation increased after phonological and semantic training but decreased after visual form training. These findings highlighted the influence of higher-level phonological and semantic associations on left occipitotemporal activation.

117There was a continued focus on the role of the left ventral occipitotemporal cortex in visual word form recognition. As previously documented, activation for processing word and word-like stimuli that have access to learnt abstract visual form representations was observed relative to unfamiliar nonword stimuli matched for visual complexity, irrespective of the hemifield of presentation and the physical form that the words were presented in and. More details of the perceptual feature-to-whole word gradient along the posterior–anterior axis of the left occipitotemporal cortex were described for both alphabetic texts and Chinese/Korean texts.

118Several studies also replicated prior observations that there was remarkable similarity in the response to visual form processing of letters, words and objects. The only studies that claimed to have found greater activation for words than pictures in the left ventral occipitotemporal cortex did not control for semantic and phonological attributes of the stimuli and used low level perceptual tasks such as the one back task (is the stimulus the same as the previous stimulus) that permit stimulus specific strategies. For example, greater activation for words, particularly in the anterior fusiform part of the ventral occipitotemporal cortex that has previously been associated with semantic processing (see Speech comprehension section above), may reflect the use of a semantic strategy for words that were not used for pictures.

119The effect of learning/experience on left ventral occipitotemporal activation was reported in two contrasting ways. In the early stages of children or adults learning to read, left ventral occipitotemporal activation increased with learning and this correlated with the rate of improvement in word recognition. However, in skilled readers, activation decreased with experience/exposure to the same stimuli and for stimuli with high relative to low orthographic familiarity and lexical frequency. These experience-dependent effects illustrate that the response in the left ventral occipitotemporal cortex changes with learning but the interpretation of the learning effect was debated.

120One interpretation is that, during the course of learning to read, the response properties of the left ventral occipitotemporal cortex (or left mid-fusiform) become selective to learnt orthographic representations with orthographic familiarity effects observed independent of phonological or semantic familiarity. Some authors further argued that specialisation for orthographic processing is at the whole word (lexical) level but agreed that orthographic processing in the left ventral occipitotemporal cortex is a precursor for mapping visual forms onto meaning and articulatory representations.

121A second perspective is that the left occipitotemporal cortex is involved in the perceptual processing of generic visual features that are present to varying degrees in all visual stimuli including words, objects, letters and faces. Within this framework, evidence was presented to support a role for the left ventral occipitotemporal cortex in (a) generic visual memory; (b) convergence of features; (c) high spatial frequencies that may bias the lateralization of processing irrespective of its higher-order properties; and (d) attention to spatial and feature processing that is related to activity in dorsal parietal regions. Although left occipitotemporal activation is not specific to written words in these accounts, specialisation for words arises in the unique network of brain regions that are activated during the word condition. In other words, the process of learning to read integrates generic visual processing with higher-order language areas and there is no need for brain areas that are specialised for orthographic processing.

122A complementary perspective is that the left ventral occipitotemporal cortex contributes to written word recognition by integrating bottom up (feed forward) generic visual processing with top-down influences from phonological, and semantic areas. After learning to read, these top-down influences are generated automatically (irrespective of task) in response to written words, but their strength can also be modulated by task and attention. This integration of visual, semantic and phonological information is not unique to written words but is required by other tasks, particularly object naming. The same left ventral occipitotemporal site also appears to function as a multi-modal integration area in the absence of visual inputs as indicated by its response during non-visual braille reading in congenitally blind participants.

123This interactive account of left ventral occipitotemporal cortical responses can explain a wide range of observations including increased activation to orthographic forms when learning to read and decreased activation as reading becomes easier. It also explains why left occipitotemporal activation is sensitive to the left-right orientation of single letters and words but not to pictures in terms of the learnt relationship between the visual form and higher-level language associations (which are orientation-specific for letters/words but not for objects). The early influence of language on visual word processing in the left ventral occipitotemporal cortex is consistent with observations that (a) the response to written words in a left-lateralized inferior frontal region (pars opercularis) peaks at the same time as that in the left ventral occipitotemporal cortex; and (b) activation during picture naming or reading aloud is reduced when the target stimulus to be named is preceded by an unconscious masked prime that has the same name as the target but a different physical form as when a word is primed by a picture or a picture is primed by a word.

124Finally, the degree to which the response in the ventral occipitotemporal cortex was left lateralized for words was found to correlate with the degree to which inferior frontal activation was left lateralized during word generation. The determinants of lateralization also varied with the subregion of occipitotemporal cortex tested. In the posterior subregion, lateralization depended on the spatial frequency of the visual inputs. In the anterior subregion, lateralization depended on the semantic demands of the task. In the middle part that has been the focus of the discussion above, lateralization was explained by decreased activation in right occipitotemporal cortex as visual expertise increased. Therefore, left lateralized activation in the ventral occipitotemporal cortex depends on the subregion tested and does not necessarily indicate a specialisation for orthography in left ventral occipitotemporal cortex.

125There is no doubt that an extensive region of the ventral occipitotemporal cortex is involved in skilled reading. Within this region, posterior areas are involved in visual feature extraction and more anterior areas are involved in lexico-semantic processing of the whole word. How the response properties in this system differ for written words and other stimuli is still a matter of debate.

126This section considers studies that have attempted to dissociate neural pathways for converting spelling (orthography) to sound (phonology) via sublexical, lexical and semantic routes. The sublexical route involves assembling the phonology associated with the whole word from its sublexical parts (sublexical orthographic to phonological conversion). The lexical route involves retrieving phonology directly from the orthography of the whole word. The semantic route involves retrieving phonology from the semantic properties of the word (similar to picture naming).

127The sublexical route is particularly important when reading new words (e.g. for pseudowords like THACY). In contrast, the lexical or semantic routes are particularly important when the sublexical spelling to sound relationships are “inconsistent” with the whole word representation (e.g. for reading irregularly spelled words like YACHT). One approach for segregating sublexical and lexical reading routes has therefore been to contrast activation for reading pseudowords with activation for reading words with irregular spellings. Another approach has been to compare reading of different alphabetic or nonalphabetic scripts that differ in the depth and consistency of their phonological clues. For example, the relationship between orthography and phonology is most consistent in Italian and least consistent in Chinese. Conversely, Chinese relies more heavily on lexical knowledge than English because Chinese is a logographic orthography that has weak phonological clues. Japanese is particularly interesting because the same words can be written in different scripts with different properties. For example, the Japanese script Kana can be read on the basis of sublexical phonological clues whereas the Japanese script Kanji must be processed at the level of morphemes (the smallest unit of meaning). Comparison of activation for different scripts (Italian versus English; English versus Chinese; Kanji versus Kana) can therefore provide clues to the neural basis of different reading pathways.

128A comparison of activation for reading the Japanese scripts Kanji and Kana found greater activation for Kanji in the posterior part of the primary visual cortex but did not find any areas that were significantly more activated for Kana. A dissociation between the scripts was, nevertheless, observed at the level of functional connectivity because, within the common set of areas that were activated for Kanji and Kana, functional connectivity was stronger in ventral reading areas for Kanji reading, and in dorsal reading areas for Kana reading. This study therefore provided evidence that morphemic reading could be differentiated from sequential (sublexical) reading. A less optimistic start was reported for the comparison of word and pseudoword reading. A double dissociation in brain activation proved to be elusive because, throughout the reading system, activation for pseudowords was greater than that for words. The interpretation for this was that activation was higher when the links between orthography and phonology were unfamiliar or unsuccessful (pseudoword reading) compared to when they were familiar and successful(real words). Critically, however, there was no report of any study that directly compared activation for reading pseudowords with activation for reading irregularly spelled words.

129Several studies compared activation for familiar words and unfamiliar pseudowords. Overall, there was a general agreement that a common neural network was activated by words and pseudowords with the most consistent difference between word types being greater activation for pseudowords, particularly in the left posterior inferior frontal cortex. One interpretation of this effect was that pseudowords increase the demands on sublexical conversion of orthography to phonology. The alternative interpretation was that pseudoword reading was more difficult. and demonstrated this by showing that left posterior inferior frontal activation was also higher for reading words with irregular spellings (e.g. KNIFE) than regular spellings (e.g. BROOM) and was proportional to response times.

130One study found that reading aloud words with irregular spellings increased activation in the left anterior ventral occipito-temporal cortex relative to reading aloud pseudowords. As irregular word reading is reliant on lexico-semantic processing, the result is consistent with prior and new claims that ventral parts of the reading system were more activated for semantic reading (Kanji) than sublexical reading (Kana).

131Plausibly, other studies of word and pseudoword reading in alphabetic scripts did not identify increased activation in the left anterior occipito-temporal cortex because they didn't specifically assess activation for words with irregular spellings or didn't scan the anterior parts of the left occipitotemporal cortex/fusiform which lie on the ventral surface of the brain and are therefore often excluded from the field of view. Evidence that a more posterior left ventral occipitotemporal area was involved in lexical compared to sublexical reading came from the observation that activation in this area was stronger in English than Italian readers,, particularly when the stimuli were pseudowords. This was interpreted in terms of reading strategy differences because Italian is a regularly spelled language and therefore sublexical links between orthography and phonology are reliable. In contrast, English is an irregularly spelled language and therefore lexical influences are always in place, even during pseudoword reading.

132Lexical and sublexical orthographic processing were also dissociated at the level of the functional interactions between shared processing areas. Specifically, demonstrated that, relative to pseudowords, words increased the functional coupling between left occipitotemporal cortex and the left ventral inferior frontal areas associated with semantic processing while decreasing the coupling between the left occipitotemporal cortex and inferior frontal regions associated with phonological processing. also distinguished different reading pathways from the occipitotemporal cortex with: a ventral pathway sustaining fast, fluent word recognition, and a dorsal pathway via the temporoparietal cortex supporting the analytic processing required for learning to integrate orthographic with phonological and semantic features of printed words. Overall, these findings were consistent with cognitive models of reading, where multiple pathways are activated by word-like stimuli with the level of activation in each pathway depending on the familiarity of the stimulus and the consistency between the orthography (letters) and phonology (sounds). There was also evidence that there might be other reading pathways in the right hemisphere particularly for reading in Chinese.

133In a meta-analysis of 35 previous neuroimaging studies of reading, dissociated two routes for reading: (a) a lexicosemantic route involving the left anterior ventral occipitotemporal cortex (basal temporal language area), the posterior part of the middle temporal gyrus, and the triangular part of inferior frontal gyrus; and (b) direct links between orthography and phonology involving left lateralized superior temporal areas, supramarginal gyrus, and the opercular part of the inferior frontal gyrus; all regions that are also involved in the articulatory loop component of short term memory which is required for phonological decisions on pseudowords.

134The involvement of an anterior fusiform/ventral occipitotemporal area in the semantic route was confirmed in a study showing that regional activation in the anterior ventral occipitotemporal cortex and the left ventral inferior frontal cortex was stronger for irregularly spelt words than pseudowords or words with regular spellings. Moreover, the functional connectivity between these two areas was also stronger for irregular words than pseudowords. Other regions associated with the semantic reading route were the left posterior temporal and parietal cortices, where activation was higher for familiar words than pseudowords and for words with irregular compared to regular spellings. Because these areas were also more activated by semantic than phonological decisions, their role in irregular word reading was again attributed to increased demands on semantic processing when sublexical access to phonology was not possible.

135While irregular word reading was associated with semantic activation, it also became evident that there was a correspondence between the areas that are more activated for reading pseudowords than real words and the areas activated by phonological relative to semantic decisions. Specifically, the left opercular part of the inferior frontal gyrus, left precentral gyrus, insular cortex, supramarginal gyrus and superior temporal areas that were more activated for phonological than semantic decisions on written words corresponded to activations that were stronger for reading pseudowords than words, for Japanese words presented in Kana relative to Kanji; for reading Spanish than English, for reading words than naming pictures and for unfamiliar than familiar words.

136An appealing interpretation of increased phonological activation for pseudowords compared to words was that it reflected the demands on accessing phonology from sublexical orthographic codes. Indeed, noted that left posterior inferior frontal activation was greater for novel words in an artificial script after new letter decoding instructions had been learnt. However, as pointed out previously by, noted that there were no areas where activation corresponded to increasing demands on phonological decoding (i.e. irregularly spelled words < regularly spelled words < pseudowords) but instead activation depended on overall response times (regularly spelled words < irregularly spelled words < pseudowords). also pointed out that left inferior frontal activation for pseudowords was not necessarily reflective of grapheme-to-phoneme conversion because this area was more activated by auditory lexical decisions on pseudo Chinese words than real Chinese words, even though the auditory task did not involve grapheme-to-phoneme conversion. Likewise, the demands on sublexical phonological processing do not easily explain why activation in the left inferior frontal cortex was higher for pseudohomophones that sound like familiar words (e.g. BRANE) than pseudowords (e.g., BLINT) that don't sound like familiar words.

137Overall, definitive interpretations of word and pseudoword activation differences were difficult because words and pseudowords differ in more than one way (e.g. visual familiarity, access to semantics and phonological decoding) and because differences in activation are only relative (rather than absolute) within areas that are commonly activated by a range of stimuli and tasks.

138Studies comparing activation for reading scripts with consistent (or transparent) and inconsistent (opaque) orthographies reported left inferior parietal or posterior superior temporal activation for more consistent orthographies (Italian and Hindi versus English; and English versus Chinese) and left middle frontal activation when phonological information was minimal or conflicting (Chinese versus English and Kanji versus Chinese). Nevertheless, predominantly common activation across all scripts and the task dependent nature of the script differences make it difficult to dissociate the anatomical components of different reading pathways on the basis of script differences alone.

139Studies comparing word and pseudoword reading within script provided further evidence that the left posterior occipitotemporal cortex was more activated by pseudowords than real words while the left anterior occipitotemporal cortex was more activated by irregular (inconsistently spelled) words than regular words. With respect to other regions in these pathways, semantic reading in the anterior ventral occipitotemporal cortex was again associated with activation in the ventral inferior frontal cortex, non-semantic serial decoding in the left supramarginal gyrus was associated with auditory short term memory and more dorsal parietal activation was associated with visual attention.

140A rather different dual route neural model of reading was proposed by who suggested that the left posterior occipitotemporal cortex was involved in sublexical processing and was only necessary for pseudoword reading. In contrast, familiar words could be read without left occipitotemporal activation by virtue of direct connectivity between occipital and parietal regions. Some support for the hypothesis that not all reading pathways involved the left ventral occipitotemporal cortex was later reported by who found evidence for links between inferior occipital and posterior superior temporal areas that were independent of activity in the left ventral occipitotemporal cortex. These studies therefore raise the interesting possibility that the left occipitotemporal cortex is not essential for accessing phonology from orthography. Future functional imaging studies are now required to test whether patients with left occipitotemporal damage who are able to read short familiar words activate the left occipital and parietal areas proposed by and/or the left occipital and superior temporal areas proposed by.

141The availability of different reading routes, for the same word stimuli, offers the potential for inter-subject variability in which routes are most strongly activated. This has been demonstrated in several studies. For example, found that, when reading a single set of familiar words, some skilled readers showed more activation in the anterior occipitotemporal–inferior frontal semantic pathway while other skilled readers showed more activation in a left posterior occipitotemporal–right inferior parietal non-semantic pathway. This and other studies have also shown that the effect of spelling-sound consistency on brain activation depends on reading skill. Another important result for disambiguating the function of different reading areas was the observation that producing the visual forms associated with articulated words (i.e. spelling to dictation) activates the left ventral occipito-temporal cortex and left pars opercularis that also sustain reading. Thus these areas are activated by both the translation of visual forms to articulation as well as the translation of articulation to visual forms.

142The clearest dissociation so far is between a lexico-semantic reading route that integrates the left ventral occipitotemporal cortex (LvOT in Table 2 and Fig. 3) with the left ventral inferior frontal gyrus, and a non-semantic phonological decoding route that links the superior temporal and ventral inferior parietal cortices to the dorsal precentral gyrus. Preliminary evidence suggests that the point of initial divergence is prior to activation in the ventral occipitotemporal area that some refer to as the visual word form area. However, it remains unclear how these pathways overlap and dissociate in the rest of the neural system for reading. My prediction is that there are multiple brain regions and multiple interconnections that underlie the reading system and these provide many possible reading pathways that are not yet appreciated in cognitive models.

143In the words of: “Modern functional brain imaging with PET and fMRI provides a new perspective on the organization of language in the human brain; a better definition of the distributed nature of the brain circuits involved, an appreciation of the flexibility of these circuits in adapting to the different aspects of speech production, an identification of areas not previously associated with the cognitive aspects of language, and a new understanding of the implications of specific brain lesions.”

144In the words of: “Modern functional brain imaging with PET and fMRI provides a new perspective on the organization of language in the human brain; a better definition of the distributed nature of the brain circuits involved, an appreciation of the flexibility of these circuits in adapting to the different aspects of speech production, an identification of areas not previously associated with the cognitive aspects of language, and a new understanding of the implications of specific brain lesions.”

145Indeed, our understanding of the functional anatomy of language has come a long way since the neurological model of Broca's and Wernicke's areas that dominated the field 20 years ago. For example, we now appreciate the importance of the cerebellum for word generation and the involvement of the basal temporal language area, anterior cingulate and left inferior prefrontal cortex in a range of different language tasks (Chertkow and Murtha, 1997). In contrast there are other areas where activation was predicted by lesion studies but not observed during functional imaging studies, such as the absence of activation in the left angular gyrus during reading aloud.

146A striking feature is that the same conclusions have been produced over and over again. Although this results in repetitive reading, it is important for validating the findings and demonstrating the remarkable consistency of the functional anatomy across individuals and studies. Yes, there are interesting and relevant sources of inter-subject variability but these are small relative to the consistent effects. The next 20 years will need to focus on understanding how different regions interact with one another and how specialisation for language arises at the level of distinct patterns of activation in areas that participate in many different functions.