Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics

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Cite this article as: eLife 2019;8:e45968 doi: 10.7554/eLife.45968

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Abstract

Sensation and action are necessarily coupled during stimulus perception - while tasting, for instance, perception happens while an animal decides to expel or swallow the substance in the mouth (the former via a behavior known as 'gaping'). Taste responses in the rodent gustatory cortex (GC) span this sensorimotor divide, progressing through firing-rate epochs that culminate in the emergence of action-related firing. Population analyses reveal this emergence to be a sudden, coherent and variably-timed ensemble transition that reliably precedes gaping onset by 0.2-0.3s. Here, we tested whether this transition drives gaping, by delivering 0.5s GC perturbations in tasting trials. Perturbations significantly delayed gaping, but only when they preceded the action-related transition - thus, the same perturbation impacted behavior or not, depending on the transition latency in that particular trial. Our results suggest a distributed attractor network model of taste processing, and a dynamical role for cortex in driving motor behavior.

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Author details

Narendra Mukherjee

Program in Neuroscience, Brandeis University, Waltham, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3808-2622
Joseph Wachutka

Program in Neuroscience, Brandeis University, Waltham, United States

Competing interests
The authors declare that no competing interests exist.
Donald B Katz

Department Of Psychology, Brandeis University, Waltham, United States

For correspondence
dbkatz@brandeis.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8444-6063

Funding

NIH Office of the Director (R01 DC006666-00)

Donald B Katz

National Science Foundation (IBN170002)

Donald B Katz

Howard Hughes Medical Institute (International Student Research Fellowship)

Narendra Mukherjee

NIH Office of the Director (R01 DC007703-06)

Donald B Katz

National Science Foundation (IBN180002)

Donald B Katz

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

Ethics

Animal experimentation: This study was performed in strict accordance with National Institute of Health guidelines and methods were approved in advance by the Brandeis University Institutional Animal Care and Use Committee in protocol numbers 15011 and 19002.

Reviewing Editor

Arianna Maffei, Stony Brook University, United States

Publication history

Received: February 10, 2019
Accepted: June 21, 2019
Accepted Manuscript published: June 24, 2019 (version 1)
Version of Record published: July 12, 2019 (version 2)

Copyright

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.