Literature DB >> 30886010

Suppressive Traveling Waves Shape Representations of Illusory Motion in Primary Visual Cortex of Awake Primate.

Sandrine Chemla1, Alexandre Reynaud1, Matteo di Volo2, Yann Zerlaut2, Laurent Perrinet1, Alain Destexhe2,3, Frédéric Chavane4.   

Abstract

How does the brain link visual stimuli across space and time? Visual illusions provide an experimental paradigm to study these processes. When two stationary dots are flashed in close spatial and temporal succession, human observers experience a percept of apparent motion. Large spatiotemporal separation challenges the visual system to keep track of object identity along the apparent motion path, the so-called "correspondence problem." Here, we use voltage-sensitive dye imaging in primary visual cortex (V1) of awake monkeys to show that intracortical connections within V1 can solve this issue by shaping cortical dynamics to represent the illusory motion. We find that the appearance of the second stimulus in V1 creates a systematic suppressive wave traveling toward the retinotopic representation of the first. Using a computational model, we show that the suppressive wave is the emergent property of a recurrent gain control fed by the intracortical network. This suppressive wave acts to explain away ambiguous correspondence problems and contributes to precisely encode the expected motion velocity at the surface of V1. Together, these results demonstrate that the nonlinear dynamics within retinotopic maps can shape cortical representations of illusory motion. Understanding these dynamics will shed light on how the brain links sensory stimuli across space and time, by preformatting population responses for a straightforward read-out by downstream areas.SIGNIFICANCE STATEMENT Traveling waves have recently been observed in different animal species, brain areas, and behavioral states. However, it is still unclear what are their functional roles. In the case of cortical visual processing, waves propagate across retinotopic maps and can hereby generate interactions between spatially and temporally separated instances of feedforward driven activity. Such interactions could participate in processing long-range apparent motion stimuli, an illusion for which no clear neuronal mechanisms have yet been proposed. Using this paradigm in awake monkeys, we show that suppressive traveling waves produce a spatiotemporal normalization of apparent motion stimuli. Our study suggests that cortical waves shape the representation of illusory moving stimulus within retinotopic maps for a straightforward read-out by downstream areas.
Copyright © 2019 the authors.

Entities:  

Keywords:  apparent motion; awake monkey; intracortical interactions; nonlinear processing; traveling waves; voltage-sensitive dye imaging

Year:  2019        PMID: 30886010      PMCID: PMC6538863          DOI: 10.1523/JNEUROSCI.2792-18.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  68 in total

1.  Parametric population representation of retinal location: neuronal interaction dynamics in cat primary visual cortex.

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Journal:  J Neurosci       Date:  1999-10-15       Impact factor: 6.167

Review 2.  Integrated model of visual processing.

Authors:  J Bullier
Journal:  Brain Res Brain Res Rev       Date:  2001-10

3.  Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps.

Authors:  P Buzás; U T Eysel; P Adorján; Z F Kisvárday
Journal:  J Comp Neurol       Date:  2001-08-27       Impact factor: 3.215

4.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons.

Authors:  James R Cavanaugh; Wyeth Bair; J Anthony Movshon
Journal:  J Neurophysiol       Date:  2002-11       Impact factor: 2.714

5.  Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys.

Authors:  Hamutal Slovin; Amos Arieli; Rina Hildesheim; Amiram Grinvald
Journal:  J Neurophysiol       Date:  2002-12       Impact factor: 2.714

6.  Contributions of the visual ventral pathway to long-range apparent motion.

Authors:  Yan Zhuo; Tian Gang Zhou; Heng Yi Rao; Jiong Jiong Wang; Ming Meng; Ming Chen; Cheng Zhou; Lin Chen
Journal:  Science       Date:  2003-01-17       Impact factor: 47.728

7.  Circuits for local and global signal integration in primary visual cortex.

Authors:  Alessandra Angelucci; Jonathan B Levitt; Emma J S Walton; Jean-Michel Hupe; Jean Bullier; Jennifer S Lund
Journal:  J Neurosci       Date:  2002-10-01       Impact factor: 6.167

8.  Imaging cortical correlates of illusion in early visual cortex.

Authors:  Dirk Jancke; Frédéric Chavane; Shmuel Naaman; Amiram Grinvald
Journal:  Nature       Date:  2004-03-25       Impact factor: 49.962

9.  Apparent motion: event-related functional magnetic resonance imaging of perceptual switches and States.

Authors:  Lars Muckli; Nikolaus Kriegeskorte; Heinrich Lanfermann; Friedhelm E Zanella; Wolf Singer; Rainer Goebel
Journal:  J Neurosci       Date:  2002-04-24       Impact factor: 6.167

10.  The visual cortical association field: a Gestalt concept or a psychophysiological entity?

Authors:  F Chavane; C Monier; V Bringuier; P Baudot; L Borg-Graham; J Lorenceau; Y Frégnac
Journal:  J Physiol Paris       Date:  2000 Sep-Dec
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  10 in total

1.  Cortical propagating waves: amplifying and suppressive?

Authors:  Matteo di Volo; Sandrine Chemla; Alain Destexhe
Journal:  J Comput Neurosci       Date:  2021-05-18       Impact factor: 1.621

2.  High-resolution VSDI retinotopic mapping via a DLP-based projection system.

Authors:  Adi Gross; Nadav H Ivzan; Nairouz Farah; Yossi Mandel
Journal:  Biomed Opt Express       Date:  2019-09-13       Impact factor: 3.732

3.  Apparent Motion Induces Activity Suppression in Early Visual Cortex and Impairs Visual Detection.

Authors:  Lu Shen; Biao Han; Floris P de Lange
Journal:  J Neurosci       Date:  2020-06-08       Impact factor: 6.167

4.  Sparse deep predictive coding captures contour integration capabilities of the early visual system.

Authors:  Victor Boutin; Angelo Franciosini; Frederic Chavane; Franck Ruffier; Laurent Perrinet
Journal:  PLoS Comput Biol       Date:  2021-01-26       Impact factor: 4.475

Review 5.  Resolving visual motion through perceptual gaps.

Authors:  Lina Teichmann; Grace Edwards; Chris I Baker
Journal:  Trends Cogn Sci       Date:  2021-09-03       Impact factor: 20.229

6.  Scene Representations Conveyed by Cortical Feedback to Early Visual Cortex Can Be Described by Line Drawings.

Authors:  Andrew T Morgan; Lucy S Petro; Lars Muckli
Journal:  J Neurosci       Date:  2019-10-14       Impact factor: 6.167

7.  A mean-field approach to the dynamics of networks of complex neurons, from nonlinear Integrate-and-Fire to Hodgkin-Huxley models.

Authors:  M Carlu; O Chehab; L Dalla Porta; D Depannemaecker; C Héricé; M Jedynak; E Köksal Ersöz; P Muratore; S Souihel; C Capone; Y Zerlaut; A Destexhe; M di Volo
Journal:  J Neurophysiol       Date:  2019-12-18       Impact factor: 2.714

8.  Emergence of Irregular Activity in Networks of Strongly Coupled Conductance-Based Neurons.

Authors:  A Sanzeni; M H Histed; N Brunel
Journal:  Phys Rev X       Date:  2022-03-08       Impact factor: 14.417

9.  Bridging Single Neuron Dynamics to Global Brain States.

Authors:  Jennifer S Goldman; Núria Tort-Colet; Matteo di Volo; Eduarda Susin; Jules Bouté; Melissa Dali; Mallory Carlu; Trang-Anh Nghiem; Tomasz Górski; Alain Destexhe
Journal:  Front Syst Neurosci       Date:  2019-12-06

10.  Nonlinear collision between propagating waves in mouse somatosensory cortex.

Authors:  M Di Volo; I Férézou
Journal:  Sci Rep       Date:  2021-10-04       Impact factor: 4.379

  10 in total

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