Communication between Brain Areas Based on Nested Oscillations

Abstract

Unraveling how brain regions communicate is crucial for understanding how the brain processes external and internal information. Neuronal oscillations within and across brain regions have been proposed to play a crucial role in this process. Two main hypotheses have been suggested for routing of information based on oscillations, namely communication through coherence and gating by inhibition. Here, we propose a framework unifying these two hypotheses that is based on recent empirical findings. We discuss a theory in which communication between two regions is established by phase synchronization of oscillations at lower frequencies (<25 Hz), which serve as temporal reference frame for information carried by high-frequency activity (>40 Hz). Our framework, consistent with numerous recent empirical findings, posits that cross-frequency interactions are essential for understanding how large-scale cognitive and perceptual networks operate.

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References 157

1. 1.

   Akam T, Kullmann DM (2014 ) Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat Rev Neurosci 15:111–122.

   Not in our library10.1038/nrn3668

2. 2.

   Angelucci A, Bullier J (2003 ) Reaching beyond the classical receptive field of VI neurons: horizontal or feedback axons?. J Physiol (Paris) 97:141–154.

   Not in our library10.1016/j.jphysparis.2003.09.001

3. 3.

   Arnal LH, Wyart V, Giraud AL (2011 ) Transitions in neural oscillations reflect prediction errors generated in audiovisual speech. Nat Neurosci 14:797–801.

   Not in our library10.1038/nn.2810

4. 4.

   Backus AR, Schoffelen J-M, Szebényi S, Hanslmayr S, Doeller CF (2016 ) Hippocampal-prefrontal theta oscillations support memory integration. Curr Biol 26:450–457.

   Not in our library10.1016/j.cub.2015.12.048

5. 5.

   Banerjee S, Snyder AC, Molholm S, Foxe JJ (2011 ) Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: supramodal or sensory-specific control mechanisms?. J Neurosci 31:9923–9932.

   Not in our library10.1523/jneurosci.4660-10.2011

6. 6.

   Barone P, Batardiere A, Knoblauch K, Kennedy H (2000 ) Laminar distribution of neurons in extrastriate areas projecting to visual areas V1 and V4 correlates with the hierarchical rank and indicates the operation of a distance rule. J Neurosci 20:3263–3281.

   Not in our library10.1523/jneurosci.20-09-03263.2000

7. 7.

   Bastos AM, Vezoli J, Bosman CA, Schoffelen JM, Oostenveld R, Dowdall JR, De Weerd P, Kennedy H, Fries P (2015 ) Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron 85:390–401.

   Not in our library10.1016/j.neuron.2014.12.018

8. 8.

   Bastos AM, Vezoli J, Fries P (2015 ) Communication through coherence with inter-areal delays. Curr Opin Neurobiol 31:173–180.

   Not in our library10.1016/j.conb.2014.11.001

9. 9.

   Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzsáki G (2012 ) Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J Neurosci 32:423–435.

   Not in our library10.1523/jneurosci.4122-11.2012

10. 10.

    Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010 ) Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66:921–936.

    Not in our library10.1016/j.neuron.2010.05.013

11. 11.

    Berman J, Liu S, Bloy L, Blaskey L, Roberts TP, Edgar JC (2014 ) Alpha-to-gamma phase-amplitude coupling methods and application to autism spectrum disorder. Brain Connect 5:80–90.

    Not in our library10.1089/brain.2014.0242

12. 12.

    Bollimunta A, Chen Y, Schroeder CE, Ding M (2008 ) Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. J Neurosci 28:9976–9988.

    Not in our library10.1523/jneurosci.2699-08.2008

13. 13.

    Bollimunta A, Mo J, Schroeder CE, Ding M (2011 ) Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J Neurosci 31:4935–4943.

    Not in our library10.1523/jneurosci.5580-10.2011

14. 14.

    Bonnefond M, Jensen O (2012 ) Alpha oscillations serve to protect working memory maintenance against anticipated distracters. Curr Biol 22:1969–1974.

    Not in our library10.1016/j.cub.2012.08.029

15. 15.

    Bonnefond M, Jensen O (2013 ) The role of gamma and alpha oscillations for blocking out distraction. Commun Integr Biol 6:e22702.

    Not in our library10.4161/cib.22702

16. 16.

    Bonnefond M, Jensen O (2015 ) Gamma activity coupled to alpha phase as a mechanism for top-down controlled gating. PLoS One 10:e0128667.

    Not in our library10.1371/journal.pone.0128667

17. 17.

    Bortone DS, Olsen SR, Scanziani M (2014 ) Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 82:474–485.

    Not in our library10.1016/j.neuron.2014.02.021

18. 18.

    Bosman CA, Womelsdorf T, Desimone R, Fries P (2009 ) A microsaccadic rhythm modulates gamma-band synchronization and behavior. J Neurosci 29:9471–9480.

    Not in our library10.1523/jneurosci.1193-09.2009

19. 19.

    Bosman CA, Schoffelen JM, Brunet N, Oostenveld R, Bastos AM, Womelsdorf T, Rubehn B, Stieglitz T, De Weerd P, Fries P (2012 ) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75:875–888.

    Not in our library10.1016/j.neuron.2012.06.037

20. 20.

    Brunet N, Vinck M, Bosman CA, Singer W, Fries P (2014 ) Gamma or no gamma, that is the question. Trends Cogn Sci 18:507–509.

    Not in our library10.1016/j.tics.2014.08.006

21. 21.
    Target-Specific Expression of Presynaptic NMDA Receptors in Neocortical Microcircuits · 2012

    No notice
22. 22.

    Buffalo EA, Fries P, Landman R, Buschman TJ, Desimone R (2011 ) Laminar differences in gamma and alpha coherence in the ventral stream. Proc Natl Acad Sci U S A 108:11262–11267.

    Not in our library10.1073/pnas.1011284108

23. 23.

    Burgess N, O’Keefe J (2011 ) Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol 21:734–744.

    Not in our library10.1016/j.conb.2011.07.002

24. 24.

    Busch NA, VanRullen R (2010 ) Spontaneous EEG oscillations reveal periodic sampling of visual attention. Proc Natl Acad Sci U S A 107:16048–16053.

    Not in our library10.1073/pnas.1004801107

25. 25.

    Buschman TJ, Denovellis EL, Diogo C, Bullock D, Miller EK (2012 ) Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76:838–846.

    Not in our library10.1016/j.neuron.2012.09.029

26. 26.

    Buzsáki G, Schomburg EW (2015 ) What does gamma coherence tell us about inter-regional neural communication? Nat Neurosci 18:484–489.

    Not in our library10.1038/nn.3952

27. 27.

    Buzsáki G, Wang X-J (2012 ) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225.

    Not in our library10.1146/annurev-neuro-062111-150444

28. 28.

    Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006 ) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628.

    Not in our library10.1126/science.1128115

29. 29.

    Canolty RT, Knight RT (2010 ) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506–515.

    Not in our library10.1016/j.tics.2010.09.001

30. 30.

    Capilla A, Schoffelen JM, Paterson G, Thut G, Gross J (2014 ) Dissociated alpha-band modulations in the dorsal and ventral visual pathways in visuospatial attention and perception. Cereb Cortex 24:550–561.

    Not in our library10.1093/cercor/bhs343

31. 31.

    Capotosto P, Babiloni C, Romani GL, Corbetta M (2009 ) Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms. J Neurosci 29:5863–5872.

    Not in our library10.1523/jneurosci.0539-09.2009

32. 32.

    Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009 ) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353–357.

    Not in our library10.1038/nature08573

33. 33.

    Colgin LL (2011 ) Oscillations and hippocampal–prefrontal synchrony. Curr Opin Neurobiol 21:467–474.

    Not in our library10.1016/j.conb.2011.04.006

34. 34.

    da Silva FH, van Lierop TH, Schrijer CF, van Leeuwen WS (1973 ) Organization of thalamic and cortical alpha rhythms: spectra and coherences. Electroencephalogr Clin Neurophysiol 35:627–639.

    Not in our library10.1016/0013-4694(73)90216-2

35. 35.

    Dotson NM, Salazar RF, Gray CM (2014 ) Frontoparietal correlation dynamics reveal interplay between integration and segregation during visual working memory. J Neurosci 34:13600–13613.

    Not in our library10.1523/jneurosci.1961-14.2014

36. 36.

    Dougherty K, Cox MA, Ninomiya T, Leopold DA, Maier A (2015 ) Ongoing alpha activity in V1 regulates visually driven spiking responses. Cereb Cortex 27:1113–1124.

    Not in our library10.1093/cercor/bhv304

37. 37.

    Drewes J, VanRullen R (2011 ) This is the rhythm of your eyes: the phase of ongoing electroencephalogram oscillations modulates saccadic reaction time. J Neurosci 31:4698–4708.

    Not in our library10.1523/jneurosci.4795-10.2011

38. 38.

    Engel AK (2012 ) Rules got rhythm. Neuron 76:673–676.

    Not in our library10.1016/j.neuron.2012.11.003

39. 39.

    Fell J, Ludowig E, Staresina BP, Wagner T, Kranz T, Elger CE, Axmacher N (2011 ) Medial temporal theta/alpha power enhancement precedes successful memory encoding: evidence based on intracranial EEG. J Neurosci 31:5392–5397.

    Not in our library10.1523/jneurosci.3668-10.2011

40. 40.

    Fiebelkorn IC, Saalmann YB, Kastner S (2013 ) Rhythmic sampling within and between objects despite sustained attention at a cued location. Curr Biol 23:2553–2558.

    Not in our library10.1016/j.cub.2013.10.063

Cited by papers we hold 5

• Nested oscillations and brain connectivity during sequential stages of feature-based attention · 2020
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• Movement-related coupling of human subthalamic nucleus spikes to cortical gamma · 2020
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• Decoding the circuitry of consciousness: From local microcircuits to brain-scale networks · 2020
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• Transcranial alternating current stimulation (tACS): from basic mechanisms towards first applications in psychiatry · 2020
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• Frequency and power of human alpha oscillations drift systematically with time-on-task · 2019
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