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Neural Oscillations and Multisensory Processing

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Advances of Multisensory Integration in the Brain

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1437))

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Abstract

Neural oscillations play a role in sensory processing by coordinating synchronized neuronal activity. Synchronization of gamma oscillations is engaged in local computation of feedforward signals and synchronization of alpha-beta oscillations is engaged in feedback processing over long-range areas. These spatially and spectrally segregated bi-directional signals may be integrated by a mechanism of cross-frequency coupling. Synchronization of neural oscillations has also been proposed as a mechanism for information integration across multiple sensory modalities. A transient stimulus or rhythmic stimulus from one modality may lead to phase alignment of ongoing neural oscillations in multiple sensory cortices, through a mechanism of cross-modal phase reset or cross-modal neural entrainment. Synchronized activities in multiple sensory cortices are more likely to boost stronger activities in downstream areas. Compared to synchronized oscillations, asynchronized oscillations may impede signal processing, and may contribute to sensory selection by setting the oscillations in the target-related cortex and the oscillations in the distractor-related cortex to opposite phases.

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References

  • Azouz R, Gray CM (2003) Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37:513–523

    Article  CAS  PubMed  Google Scholar 

  • Baldauf D, Desimone R (2014) Neural mechanisms of object-based attention. Science 344:424–427

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bauer AR, Debener S, Nobre AC (2020) Synchronisation of neural oscillations and cross-modal influences. Trends Cogn Sci 24:481–495

    Article  PubMed  PubMed Central  Google Scholar 

  • Bressler SL, Richter CG (2015) Interareal oscillatory synchronization in top-down neocortical processing. Curr Opin Neurobiol 31:62–66

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Cappe C, Morel A, Rouiller EM (2007) Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys. Neuroscience 146:1371–1387

    Article  CAS  PubMed  Google Scholar 

  • Cecere R, Rees G, Romei V (2015) Individual differences in alpha frequency drive crossmodal illusory perception. Curr Biol 25:231–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demiralp T, Bayraktaroglu Z, Lenz D, Junge S, Busch NA, Maess B, Ergen M, Herrmann CS (2007) Gamma amplitudes are coupled to theta phase in human EEG during visual perception. Int J Psychophysiol 64:24–30

    Article  PubMed  Google Scholar 

  • Desimone R, Duncan J (1995) Neural Mechanisms of Selective Visual Attention. Annual Review of Neuroscience 18(1):193–222

    Google Scholar 

  • Diederich A, Schomburg A, Colonius H (2012) Saccadic reaction times to audiovisual stimuli show effects of oscillatory phase reset. PLoS One 7:e44910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419–451

    Article  CAS  PubMed  Google Scholar 

  • Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57:11–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318:1147–1150

    Article  CAS  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

    Article  CAS  PubMed  Google Scholar 

  • Fiebelkorn IC, Snyder AC, Mercier MR, Butler JS, Molholm S, Foxe JJ (2013) Cortical cross-frequency coupling predicts perceptual outcomes. NeuroImage 69:126–137

    Article  CAS  PubMed  Google Scholar 

  • Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480

    Article  PubMed  Google Scholar 

  • Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88:220–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278–285

    Article  PubMed  Google Scholar 

  • Gutig R (2014) To spike, or when to spike? Curr Opin Neurobiol 25:134–139

    Article  PubMed  Google Scholar 

  • Hackett TA, De La Mothe LA, Ulbert I, Karmos G, Smiley J, Schroeder CE (2007) Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane. J Comp Neurol 502:924–952

    Article  PubMed  Google Scholar 

  • Ibrahim LA, Mesik L, Ji X-Y, Fang Q, Li H-F, Li Y-T, Zingg B, Zhang LI, Tao HW (2016) Cross-modality sharpening of visual cortical processing through layer-1-mediated inhibition and disinhibition. Neuron 89:1031–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaramillo J, Kempter R (2017) Phase precession: a neural code underlying episodic memory? Curr Opin Neurobiol 43:130–138

    Article  CAS  PubMed  Google Scholar 

  • Jones MR, Moynihan H, MacKenzie N, Puente J (2002) Temporal aspects of stimulus-driven attending in dynamic arrays. Psychol Sci 13:313–319

    Article  PubMed  Google Scholar 

  • Kambe J, Kakimoto Y, Araki O (2015) Phase reset affects auditory-visual simultaneity judgment. Cogn Neurodyn 9:487–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Kann O, Papageorgiou IE, Draguhn A (2014) Highly energized inhibitory interneurons are a central element for information processing in cortical networks. J Cereb Blood Flow Metab 34:1270–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayser C, Petkov CI, Augath M, Logothetis NK (2007) Functional imaging reveals visual modulation of specific fields in auditory cortex. J Neurosci 27:1824–1835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayser C, Petkov CI, Logothetis NK (2008) Visual modulation of neurons in auditory cortex. Cereb Cortex 18:1560–1574

    Article  PubMed  Google Scholar 

  • Keil J, Senkowski D (2018) Neural oscillations orchestrate multisensory processing. Neuroscientist 24:609–626

    Article  PubMed  Google Scholar 

  • Konig P, Engel AK, Singer W (1996) Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci 19:130–137

    Article  CAS  PubMed  Google Scholar 

  • Krebber M, Harwood J, Spitzer B, Keil J, Senkowski D (2015) Visuotactile motion congruence enhances gamma-band activity in visual and somatosensory cortices. NeuroImage 117:160–169

    Article  PubMed  Google Scholar 

  • Lakatos P, Chen CM, O’Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320:110–113

    Article  CAS  PubMed  Google Scholar 

  • Lakatos P, O’Connell MN, Barczak A, Mills A, Javitt DC, Schroeder CE (2009) The leading sense: supramodal control of neurophysiological context by attention. Neuron 64:419–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JH, Whittington MA, Kopell NJ (2013) Top-down beta rhythms support selective attention via interlaminar interaction: a model. PLoS Comput Biol 9:e1003164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livingstone MS (1996) Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex. J Neurophysiol 75:2467–2485

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier A, Adams GK, Aura C, Leopold DA (2010) Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front Syst Neurosci 4

    Google Scholar 

  • Markov NT, Vezoli J, Chameau P, Falchier A, Quilodran R, Huissoud C, Lamy C, Misery P, Giroud P, Ullman S et al (2014) Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J Comp Neurol 522:225–259

    Article  PubMed  Google Scholar 

  • Mathewson KE, Fabiani M, Gratton G, Beck DM, Lleras A (2010) Rescuing stimuli from invisibility: inducing a momentary release from visual masking with pre-target entrainment. Cognition 115:186–191

    Article  PubMed  Google Scholar 

  • Mercier MR, Foxe JJ, Fiebelkorn IC, Butler JS, Schwartz TH, Molholm S (2013) Auditory-driven phase reset in visual cortex: human electrocorticography reveals mechanisms of early multisensory integration. NeuroImage 79:19–29

    Article  PubMed  Google Scholar 

  • Mercier MR, Molholm S, Fiebelkorn IC, Butler JS, Schwartz TH, Foxe JJ (2015) Neuro-oscillatory phase alignment drives speeded multisensory response times: an electro-corticographic investigation. J Neurosci 35:8546–8557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meredith MA, Stein BE (1996) Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75:1843–1857

    Article  CAS  PubMed  Google Scholar 

  • Michalareas G, Vezoli J, van Pelt S, Schoffelen JM, Kennedy H, Fries P (2016) Alpha-Beta and Gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron 89:384–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JE, Carlson LA, McAuley JD (2013) When what you hear influences when you see: listening to an auditory rhythm influences the temporal allocation of visual attention. Psychol Sci 24:11–18

    Article  PubMed  Google Scholar 

  • Moran J, Desimone R (1985) Selective Attention Gates Visual Processing in the Extrastriate Cortex. Science 229(4715):782–784

    Google Scholar 

  • Naue N, Rach S, Struber D, Huster RJ, Zaehle T, Korner U, Herrmann CS (2011) Auditory event-related response in visual cortex modulates subsequent visual responses in humans. J Neurosci 31:7729–7736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palva JM, Palva S (2018) Functional integration across oscillation frequencies by cross-frequency phase synchronization. Eur J Neurosci 48:2399–2406

    Article  PubMed  Google Scholar 

  • Palva JM, Palva S, Kaila K (2005) Phase synchrony among neuronal oscillations in the human cortex. J Neurosci 25:3962–3972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perrodin C, Kayser C, Logothetis NK, Petkov CI (2015) Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex. Proc Natl Acad Sci U S A 112:273–278

    Article  CAS  PubMed  Google Scholar 

  • Plass J, Ahn E, Towle VL, Stacey WC, Wasade VS, Tao J, Wu S, Issa NP, Brang D (2019) Joint encoding of auditory timing and location in visual cortex. J Cogn Neurosci 31:1002–1017

    Article  PubMed  PubMed Central  Google Scholar 

  • Richter CG, Thompson WH, Bosman CA, Fries P (2017) Top-down beta enhances bottom-up gamma. J Neurosci 37:6698–6711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizzuto DS, Madsen JR, Bromfield EB, Schulze-Bonhage A, Kahana MJ (2006) Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. NeuroImage 31:1352–1358

    Article  PubMed  Google Scholar 

  • Romei V, Gross J, Thut G (2012) Sounds reset rhythms of visual cortex and corresponding human visual perception. Curr Biol 22:807–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roopun AK, Kramer MA, Carracedo LM, Kaiser M, Davies CH, Traub RD, Kopell NJ, Whittington MA (2008) Period concatenation underlies interactions between gamma and beta rhythms in neocortex. Front Cell Neurosci 2:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenblum MG, Weule J, Kurths J, Pickovsky A, Volkmann J, Schnitzler A, Freund HJ (1998) Detection of n:m phase locking from noisy data: application to magnetoencephalography. Phys Rev Lett 81:3291–3294

    Article  Google Scholar 

  • Saleh M, Reimer J, Penn R, Ojakangas CL, Hatsopoulos NG (2010) Fast and slow oscillations in human primary motor cortex predict oncoming behaviorally relevant cues. Neuron 65:461–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoffelen J, Oostenveld R, Fries P (2005) Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308:111–114

    Article  CAS  PubMed  Google Scholar 

  • Schroeder CE, Foxe J (2005) Multisensory contributions to low-level, ‘unisensory’ processing. Curr Opin Neurobiol 15:454–458

    Article  CAS  PubMed  Google Scholar 

  • Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9–18

    Article  CAS  PubMed  Google Scholar 

  • Senkowski D, Schneider TR, Foxe JJ, Engel AK (2008) Crossmodal binding through neural coherence: implications for multisensory processing. Trends Neurosci 31:401–409

    Article  CAS  PubMed  Google Scholar 

  • Simon DM, Wallace MT (2017) Rhythmic modulation of entrained auditory oscillations by visual inputs. Brain Topogr 30:565–578

    Article  PubMed  Google Scholar 

  • Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586

    Article  CAS  PubMed  Google Scholar 

  • Smith MA, Jia X, Zandvakili A, Kohn A (2013) Laminar dependence of neuronal correlations in visual cortex. J Neurophysiol 109:940–947

    Article  PubMed  Google Scholar 

  • Stein BE, Meredith MA, Wallace MT (1993) The visually responsive neuron and beyond: multisensory integration in cat and monkey. Prog Brain Res 95:79–90

    Article  CAS  PubMed  Google Scholar 

  • Swadlow HA, Gusev AG (2001) The impact of ‘bursting’ thalamic impulses at a neocortical synapse. Nat Neurosci 4:402–408

    Article  CAS  PubMed  Google Scholar 

  • Tamas G, Buhl EH, Lorincz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366–371

    Article  CAS  PubMed  Google Scholar 

  • Treue S, Maunsell J H (1996) Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382(6591):539–541

    Google Scholar 

  • van Atteveldt N, Murray MM, Thut G, Schroeder CE (2014) Multisensory integration: flexible use of general operations. Neuron 81:1240–1253

    Article  PubMed  PubMed Central  Google Scholar 

  • van Kerkoerle T, Self MW, Dagnino B, Gariel-Mathis MA, Poort J, van der Togt C, Roelfsema PR (2014) Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc Natl Acad Sci U S A 111:14332–14341

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanhatalo S, Palva JM, Holmes MD, Miller JW, Voipio J, Kaila K (2004) Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. Proc Natl Acad Sci U S A 101:5053–5057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voytek B, Canolty RT, Shestyuk A, Crone NE, Parvizi J, Knight RT (2010) Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Front Hum Neurosci 4:191

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Xu M, Kamigaki T, Hoang Do JP, Chang WC, Jenvay S, Miyamichi K, Luo L, Dan Y (2014) Long-range and local circuits for top-down modulation of visual cortex processing You only see what you want to see. Science 345(6197):660–665

    Google Scholar 

  • Zuo Y, Huang Y, Wu D, Wang Q, Wang Z (2020) Spike phase shift relative to Beta oscillations mediates modality selection. Cereb Cortex 30:5431–5448

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by National Science and Technology Innovation 2030 Major Program of China (grant No. STI2030-Major Projects 2021ZD0203700/2021ZD0203703) and National Nature Science Foundation of China (Grant No. 32271077) to Yanfang Zuo.

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Authors and Affiliations

  1. Department of Neurology, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology, Guangzhou, China

    Yanfang Zuo

  2. Center for Medical Research on Innovation and Translation, Institute of Clinical Medicine, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology, Guangzhou, China

    Yanfang Zuo

  3. Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science & Intelligence Technology, Chinese Academy of Sciences, Shanghai, China

    Zuoren Wang

  4. University of Chinese Academy of Sciences, Beijing, China

    Zuoren Wang

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  1. Yanfang Zuo
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  2. Zuoren Wang
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Editors and Affiliations

  1. Systems Neuroscience, Institute of Neuroscience Chinese Academy of Sciences, Shanghai, China

    Yong Gu

  2. Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat Gan, Israel

    Adam Zaidel

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Zuo, Y., Wang, Z. (2024). Neural Oscillations and Multisensory Processing. In: Gu, Y., Zaidel, A. (eds) Advances of Multisensory Integration in the Brain. Advances in Experimental Medicine and Biology, vol 1437. Springer, Singapore. https://doi.org/10.1007/978-981-99-7611-9_8

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