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Interneuron specific gamma synchronization indexes cue uncertainty and prediction errors in lateral prefrontal and anterior cingulate cortex

  1. Kianoush Banaie Boroujeni  Is a corresponding author
  2. Paul Tiesinga
  3. Thilo Womelsdorf  Is a corresponding author
  1. Vanderbilt University, United States
  2. Donders Institute, Netherlands
Research Article
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Cite this article as: eLife 2021;10:e69111 doi: 10.7554/eLife.69111

Abstract

Inhibitory interneurons are believed to realize critical gating functions in cortical circuits, but it has been difficult to ascertain the content of gated information for well characterized interneurons in primate cortex. Here, we address this question by characterizing putative interneurons in primate prefrontal and anterior cingulate cortex while monkeys engaged in attention demanding reversal learning. We find that subclasses of narrow spiking neurons have a relative suppressive effect on the local circuit indicating they are inhibitory interneurons. One of these interneuron subclasses showed prominent firing rate modulations and (35-45 Hz) gamma synchronous spiking during periods of uncertainty in both, lateral prefrontal cortex (LPFC) and in anterior cingulate cortex (ACC). In LPFC this interneuron subclass activated when the uncertainty of attention cues was resolved during flexible learning, whereas in ACC it fired and gamma-synchronized when outcomes were uncertain and prediction errors were high during learning. Computational modeling of this interneuron-specific gamma band activity in simple circuit motifs suggests it could reflect a soft winner-take-all gating of information having high degree of uncertainty. Together, these findings elucidate an electrophysiologically-characterized interneuron subclass in the primate, that forms gamma synchronous networks in two different areas when resolving uncertainty during adaptive goal-directed behavior.

Data availability

Source neural data and matlab scripts for reproducing the main figures with the data are included in the manuscript as supporting files Source Data 1, 2, and 3.

Article and author information

Author details

  1. Kianoush Banaie Boroujeni

    Psychology, Vanderbilt University, Nashville, United States
    For correspondence
    kianoush.banaie.boroujeni@vanderbilt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2323-0648
  2. Paul Tiesinga

    Donders Institute, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Thilo Womelsdorf

    Psychology, Vanderbilt University, Nashville, United States
    For correspondence
    thilo.womelsdorf@vanderbilt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6921-4187

Funding

National Institute of Mental Health (R01MH123687)

  • Thilo Womelsdorf

Canadian Institutes of Health Research (MOP 102482)

  • Thilo Womelsdorf

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 animal care and experimental protocols were approved by the York University Council on Animal Care (ethics protocol 2015-15-R2) and were in accordance with the Canadian Council on Animal Care guidelines.

Reviewing Editor

  1. Saskia Haegens, Columbia University College of Physicians and Surgeons, United States

Publication history

  1. Received: April 5, 2021
  2. Accepted: June 17, 2021
  3. Accepted Manuscript published: June 18, 2021 (version 1)
  4. Version of Record published: July 1, 2021 (version 2)

Copyright

© 2021, Banaie Boroujeni 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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