Attentional modulation of neuronal variability in circuit models of cortex

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Abstract

The circuit mechanisms behind shared neural variability (noise correlation) and its dependence on neural state are poorly understood. Visual attention is well-suited to constrain cortical models of response variability because attention both increases firing rates and their stimulus sensitivity, as well as decreases noise correlations. We provide a novel analysis of population recordings in rhesus primate visual area V4 showing that a single biophysical mechanism may underlie these diverse neural correlates of attention. We explore model cortical networks where top-down mediated increases in excitability, distributed across excitatory and inhibitory targets, capture the key neuronal correlates of attention. Our models predict that top-down signals primarily affect inhibitory neurons, whereas excitatory neurons are more sensitive to stimulus specific bottom-up inputs. Accounting for trial variability in models of state dependent modulation of neuronal activity is a critical step in building a mechanistic theory of neuronal cognition.

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Tatjana Kanashiro

Program for Neural Computation, Carnegie Mellon University and University of Pittsburgh, Pittsburgh, United States

Competing interests
The authors declare that no competing interests exist.
Gabriel Koch Ocker

Department of Mathematics, University of Pittsburgh, Pittsburgh, United States

Competing interests
The authors declare that no competing interests exist.
Marlene R Cohen

Center for the Neural Basis of Cognition, Pittsburgh, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8583-4300
Brent Doiron

Department of Mathematics, University of Pittsburgh, Pittsburgh, United States

For correspondence
bdoiron@pitt.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6916-5511

Funding

Simons Collaboration on the Global Brain

Marlene R Cohen
Brent Doiron

National Institutes of Health (R01 EY022930)

Marlene R Cohen

National Science Foundation (DMS-1313225)

Tatjana Kanashiro
Gabriel Koch Ocker
Brent Doiron

National Science Foundation (DMS-1517082)

Gabriel Koch Ocker
Brent Doiron

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 procedures were in accordance with the Institutional Animal Care and Use Committee of Harvard Medical School (Harvard IACUC protocol number: 04214).

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.