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Anticipatory responses along motion trajectories in awake monkey area V1

View ORCID ProfileGiacomo Benvenuti, Sandrine Chemla, Arjan Boonman, View ORCID ProfileLaurent Perrinet, View ORCID ProfileGuillaume S Masson, Frédéric Chavane
doi: https://doi.org/10.1101/2020.03.26.010017
Giacomo Benvenuti
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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  • ORCID record for Giacomo Benvenuti
Sandrine Chemla
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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Arjan Boonman
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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Laurent Perrinet
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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Guillaume S Masson
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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Frédéric Chavane
1Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin, Marseille 13005, France
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  • For correspondence: frederic.chavane@univ-amu.fr
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ABSTRACT

What are the neural mechanisms underlying motion integration of translating objects? Visual motion integration is generally conceived of as a feedforward, hierarchical, information processing. However, feedforward models fail to account for many contextual effects revealed using natural moving stimuli. In particular, a translating object evokes a sequence of transient feedforward responses in the primary visual cortex but also propagations of activity through horizontal and feedback pathways. We investigated how these pathways shape the representation of a translating bar in monkey V1. We show that, for long trajectories, spiking activity builds-up hundreds of milliseconds before the bar enters the neurons’ receptive fields. Using VSDI and LFP recordings guided by a phenomenological model of propagation dynamics, we demonstrate that this anticipatory response arises from the interplay between horizontal and feedback networks driving V1 neurons well ahead of their feedforward inputs. This mechanism could subtend several perceptual contextual effects observed with translating objects.

Highlights

  • Our hypothesis is that lateral propagation of activity in V1 contributes to the integration of translating stimuli

  • Consistent with this hypothesis, we find that a translating bar induces anticipatory spiking activity in V1 neurons.

  • A V1 model describes how this anticipation can arise from inter and intra-cortical lateral propagation of activity.

  • The dynamic of VSDi and LFP signals in V1 is consistent with the predictions made by the model.

  • The intra-cortical origin is further confirmed by the fact that a bar moving from the ipsilateral hemifield does not evoke anticipation.

  • Horizontal and feedback input are not only modulatory but can also drive spiking responses in specific contexts.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 29, 2020.
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Anticipatory responses along motion trajectories in awake monkey area V1
Giacomo Benvenuti, Sandrine Chemla, Arjan Boonman, Laurent Perrinet, Guillaume S Masson, Frédéric Chavane
bioRxiv 2020.03.26.010017; doi: https://doi.org/10.1101/2020.03.26.010017
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Anticipatory responses along motion trajectories in awake monkey area V1
Giacomo Benvenuti, Sandrine Chemla, Arjan Boonman, Laurent Perrinet, Guillaume S Masson, Frédéric Chavane
bioRxiv 2020.03.26.010017; doi: https://doi.org/10.1101/2020.03.26.010017

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