Effects of Sensorineural Hearing Loss on Cortical Synchronization to Competing Speech during Selective Attention

Abstract

When selectively attending to a speech stream in multi-talker scenarios, low-frequency cortical activity is known to synchronize selectively to fluctuations in the attended speech signal. Older listeners with age-related sensorineural hearing loss (presbycusis) often struggle to understand speech in such situations, even when wearing a hearing aid. Yet, it is unclear whether a peripheral hearing loss degrades the attentional modulation of cortical speech tracking. Here, we used psychoacoustics and electroencephalography (EEG) in male and female human listeners to examine potential effects of hearing loss on EEG correlates of speech envelope synchronization in cortex. Behaviorally, older hearing-impaired (HI) listeners showed degraded speech-in-noise recognition and reduced temporal acuity compared with age-matched normal-hearing (NH) controls. During EEG recordings, we used a selective attention task with two spatially separated simultaneous speech streams where NH and HI listeners both showed high speech recognition performance. Low-frequency (<10 Hz) envelope-entrained EEG responses were enhanced in the HI listeners, both for the attended speech, but also for tone sequences modulated at slow rates (4 Hz) during passive listening. Compared with the attended speech, responses to the ignored stream were found to be reduced in both HI and NH listeners, allowing for the attended target to be classified from single-trial EEG data with similar high accuracy in the two groups. However, despite robust attention-modulated speech entrainment, the HI listeners rated the competing speech task to be more difficult. These results suggest that speech-in-noise problems experienced by older HI listeners are not necessarily associated with degraded attentional selection. SIGNIFICANCE STATEMENT People with age-related sensorineural hearing loss often struggle to follow speech in the presence of competing talkers. It is currently unclear whether hearing impairment may impair the ability to use selective attention to suppress distracting speech in situations when the distractor is well segregated from the target. Here, we report amplified envelope-entrained cortical EEG responses to attended speech and to simple tones modulated at speech rates (4 Hz) in listeners with age-related hearing loss. Critically, despite increased self-reported listening difficulties, cortical synchronization to speech mixtures was robustly modulated by selective attention in listeners with hearing loss. This allowed the attended talker to be classified from single-trial EEG responses with high accuracy in both older hearing-impaired listeners and age-matched normal-hearing controls.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 87

1. 1.

   Aiken SJ, Picton TW (2008 ) Human cortical responses to the speech envelope. Ear Hear 29:139–157.

   Not in our library10.1097/aud.0b013e31816453dc

2. 2.

   Akeroyd MA (2008 ) Are individual differences in speech reception related to individual differences in cognitive ability? A survey of twenty experimental studies with normal and hearing-impaired adults. Int J Audiol 47:S53–S71.

   Not in our library10.1080/14992020802301142

3. 3.

   Alain C, Roye A, Salloum C (2014 ) Effects of age-related hearing loss and background noise on neuromagnetic activity from auditory cortex. Front Syst Neurosci 8:8.

   Not in our library10.3389/fnsys.2014.00008

4. 4.

   Andrés P, Parmentier FB, Escera C (2006 ) The effect of age on involuntary capture of attention by irrelevant sounds: a test of the frontal hypothesis of aging. Neuropsychologia 44:2564–2568.

   Not in our library10.1016/j.neuropsychologia.2006.05.005

5. 5.

   Barsz K, Wilson WW, Walton JP (2007 ) Reorganization of receptive fields following hearing loss in inferior colliculus neurons. Neuroscience 147:532–545.

   Not in our library10.1016/j.neuroscience.2007.04.031

6. 6.

   Benjamini Y, Hochberg Y (1995 ) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300.

   Not in our library

7. 7.

   Billings CJ, Madsen BM (2018 ) A perspective on brain-behavior relationships and effects of age and hearing using speech-in-noise stimuli. Hear Res 369:90–102.

   Not in our library10.1016/j.heares.2018.03.024

8. 8.

   Bisgaard N, Vlaming MS, Dahlquist M (2010 ) Standard audiograms for the IEC 60118–15 measurement procedure. Trends Amplif 14:113–120.

   Not in our library10.1177/1084713810379609

9. 9.

   Blackburn HL, Benton AL (1957 ) Revised administration and scoring of the digit span test. J Consult Psychol 21:139.

   Not in our library10.1037/h0047235

10. 10.

    Carney LH (2018 ) Supra-threshold hearing and fluctuation profiles: implications for sensorineural and hidden hearing loss. J Assoc Res Otolaryngol 19:331–352.

    Not in our library10.1007/s10162-018-0669-5

11. 11.

    Caspary DM, Ling L, Turner JG, Hughes LF (2008 ) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791.

    Not in our library10.1242/jeb.013581

12. 12.

    Caspary DM, Hughes LF, Ling LL (2013 ) Age-related GABAA receptor changes in rat auditory cortex. Neurobiol Aging 34:1486–1496.

    Not in our library10.1016/j.neurobiolaging.2012.11.009

13. 13.

    Chambers AR, Resnik J, Yuan Y, Whitton JP, Edge AS, Liberman MC, Polley DB (2016 ) Central gain restores auditory processing following near-complete cochlear denervation. Neuron 89:867–879.

    Not in our library10.1016/j.neuron.2015.12.041

14. 14.

    Dai L, Best V, Shinn-Cunningham BG (2018 ) Sensorineural hearing loss degrades behavioral and physiological measures of human spatial selective auditory attention. Proc Natl Acad Sci U S A 115:E3286–E3295.

    Not in our library10.1073/pnas.1721226115

15. 15.

    de Cheveigné A, Parra LC (2014 ) Joint decorrelation, a versatile tool for multichannel data analysis. Neuroimage 98:487–505.

    Not in our library10.1016/j.neuroimage.2014.05.068

16. 16.

    Di Liberto GM, O'Sullivan JA, Lalor EC (2015 ) Low-frequency cortical entrainment to speech reflects phoneme-level processing. Curr Biol 25:2457–2465.

    Not in our library10.1016/j.cub.2015.08.030

17. 17.

    Ding N, Simon JZ (2012a ) Neural coding of continuous speech in auditory cortex during monaural and dichotic listening. J Neurophysiol 107:78–89.

    Not in our library10.1152/jn.00297.2011

18. 18.

    Ding N, Simon JZ (2012b ) Emergence of neural encoding of auditory objects while listening to competing speakers. Proc Natl Acad Sci U S A 109:11854–11859.

    Not in our library10.1073/pnas.1205381109

19. 19.

    Ding N, Simon JZ (2013 ) Adaptive temporal encoding leads to a background-insensitive cortical representation of speech. J Neurosci 33:5728–5735.

    Not in our library10.1523/jneurosci.5297-12.2013

20. 20.
    Interaction between Attention and Bottom-Up Saliency Mediates the Representation of Foreground and Background in an Auditory Scene · 2009

    No notice
21. 21.
    The Speech, Spatial and Qualities of Hearing Scale (SSQ) · 2004

    No notice
22. 22.

    Gazzaley A, Cooney JW, Rissman J, D'Esposito M (2005 ) Top-down suppression deficit underlies working memory impairment in normal aging. Nat Neurosci 8:1298–1300.

    Not in our library10.1038/nn1543

23. 23.

    Gazzaley A, Clapp W, Kelley J, McEvoy K, Knight RT, D'Esposito M (2008 ) Age-related top-down suppression deficit in the early stages of cortical visual memory processing. Proc Natl Acad Sci U S A 105:13122–13126.

    Not in our library10.1073/pnas.0806074105

24. 24.

    Gerken GM (1979 ) Central denervation hypersensitivity in the auditory system of the cat. J Acoust Soc Am 66:721–727.

    Not in our library10.1121/1.383222

25. 25.

    Glasberg BR, Moore BC (1990 ) Derivation of auditory filter shapes from notched-noise data. Hear Res 47:103–138.

    Not in our library10.1016/0378-5955(90)90170-t

26. 26.

    Goossens T, Vercammen C, Wouters J, van Wieringen A (2016 ) Aging affects neural synchronization to speech-related acoustic modulations. Front Aging Neurosci 8:133.

    Not in our library10.3389/fnagi.2016.00133

27. 27.

    Goossens T, Vercammen C, Wouters J, van Wieringen A (2018 ) Neural envelope encoding predicts speech perception performance for normal-hearing and hearing-impaired adults. Hear Res 370:189–200.

    Not in our library10.1016/j.heares.2018.07.012

28. 28.

    Goossens T, Vercammen C, Wouters J, van Wieringen A (2019 ) The association between hearing impairment and neural envelope encoding at different ages. Neurobiol Aging 74:202–212.

    Not in our library10.1016/j.neurobiolaging.2018.10.008

29. 29.

    Grimault N, Micheyl C, Carlyon RP, Arthaud P, Collet L (2001 ) Perceptual auditory stream segregation of sequences of complex sounds in subjects with normal and impaired hearing. Br J Audiol 35:173–182.

    Not in our library10.1080/00305364.2001.11745235

30. 30.

    Heeringa AN, van Dijk P (2019 ) Neural coding of the sound envelope is changed in the inferior colliculus immediately following acoustic trauma. Eur J Neurosci 49:1220–1232.

    Not in our library10.1111/ejn.14299

31. 31.

    Herrmann B, Parthasarathy A, Bartlett EL (2017 ) Ageing affects dual encoding of periodicity and envelope shape in rat inferior colliculus neurons. Eur J Neurosci 45:299–311.

    Not in our library10.1111/ejn.13463

32. 32.

    Herrmann B, Buckland C, Johnsrude IS (2019 ) Neural signatures of temporal regularity processing in sounds differ between younger and older adults. Neurobiol Aging 83:73–85.

    Not in our library10.1016/j.neurobiolaging.2019.08.028

33. 33.

    Hughes LF, Turner JG, Parrish JL, Caspary DM (2010 ) Processing of broadband stimuli across A1 layers in young and aged rats. Hear Res 264:79–85.

    Not in our library10.1016/j.heares.2009.09.005

34. 34.

    Kale S, Heinz MG (2010 ) Envelope coding in auditory nerve fibers following noise-induced hearing loss. J Assoc Res Otolaryngol 11:657–673.

    Not in our library10.1007/s10162-010-0223-6

35. 35.

    Kochkin S (2005 ) MarkeTrak VII: customer satisfaction with hearing instruments in the digital age. Hear J 58:30–32.

    Not in our library10.1097/01.hj.0000286545.33961.e7

36. 36.

    Kong YY, Somarowthu A, Ding N (2015 ) Effects of spectral degradation on attentional modulation of cortical auditory responses to continuous speech. J Assoc Res Otolaryngol 16:783–796.

    Not in our library10.1007/s10162-015-0540-x

37. 37.

    Larsby B, Arlinger S (1999 ) Auditory temporal and spectral resolution in normal and impaired hearing. J Am Acad Audiol 10:198–210.

    Not in our library

38. 38.

    Luo H, Poeppel D (2007 ) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54:1001–1010.

    Not in our library10.1016/j.neuron.2007.06.004

39. 39.

    Millman RE, Mattys SL, Gouws AD, Prendergast G (2017 ) Magnified neural envelope coding predicts deficits in speech perception in noise. J Neurosci 37:7727–7736.

    Not in our library10.1523/jneurosci.2722-16.2017

40. 40.

    Mirkovic B, Bleichner MG, De Vos M, Debener S (2016 ) Target speaker detection with concealed EEG around the ear. Front Neurosci 10:349.

    Not in our library10.3389/fnins.2016.00349

Cited by papers we hold 2

• Age-related hearing loss is associated with alterations in temporal envelope processing in different neural generators along the auditory pathway · 2022
  Not checked
• Brain-informed speech separation (BISS) for enhancement of target speaker in multitalker speech perception · 2020
  Not checked

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.