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Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations

  1. Alina Peter
  2. Cem Uran
  3. Johanna Klon-Lipok
  4. Rasmus Roese
  5. Sylvia van Stijn
  6. William Barnes
  7. Jarrod R Dowdall
  8. Wolf Singer
  9. Pascal Fries
  10. Martin Vinck  Is a corresponding author
  1. Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
  2. Max Planck Institute for Brain Research, Germany
Research Article
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Cite this article as: eLife 2019;8:e42101 doi: 10.7554/eLife.42101

Abstract

The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30-80Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma-synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma-synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context.

Article and author information

Author details

  1. Alina Peter

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8497-6235
  2. Cem Uran

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Johanna Klon-Lipok

    Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Rasmus Roese

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Sylvia van Stijn

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. William Barnes

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3833-1214
  7. Jarrod R Dowdall

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Wolf Singer

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Pascal Fries

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Martin Vinck

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    For correspondence
    martin.vinck@esi-frankfurt.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4044-0970

Funding

Deutsche Forschungsgemeinschaft (SPP 1665)

  • Pascal Fries

European Commission (FP7-604102-HBP)

  • Pascal Fries

Deutsche Forschungsgemeinschaft (FOR 1847)

  • Pascal Fries

Deutsche Forschungsgemeinschaft (FR2557/5-1-CORNET)

  • Pascal Fries

Deutsche Forschungsgemeinschaft (FR2557/6-1-NeuroTMR)

  • Pascal Fries

Deutsche Forschungsgemeinschaft (Reinhart Kosselleck grant)

  • Wolf Singer

National Institutes of Health (1U54MH091657-WU-Minn- Consortium-HCP)

  • Pascal Fries

European Science Foundation (European Young Investigator Award)

  • Pascal Fries

LOEWE (NeFF)

  • Pascal Fries

European Commission (HEALTH-F2-2008-200728-BrainSynch)

  • Pascal Fries

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures complied with the German and European regulations for the protection of animals and were approved by the regional authority (Regierungspräsidium Darmstadt, F-149-1000/1005). All surgeries were performed under anesthesia and were followed by analgesic treatment post-operatively.

Reviewing Editor

  1. Laura Colgin, The University of Texas at Austin, United States

Publication history

  1. Received: September 18, 2018
  2. Accepted: January 30, 2019
  3. Accepted Manuscript published: February 4, 2019 (version 1)

Copyright

© 2019, Peter et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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