Attentional modulation of neuronal variability in circuit models of cortex

  1. Tatjana Kanashiro
  2. Gabriel Koch Ocker
  3. Marlene R Cohen
  4. Brent Doiron  Is a corresponding author
  1. Carnegie Mellon University and University of Pittsburgh, United States
  2. University of Pittsburgh, United States
  3. Center for the Neural Basis of Cognition, United States

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.

Article and author information

Author details

  1. 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.
  2. Gabriel Koch Ocker

    Department of Mathematics, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Marlene R Cohen

    Center for the Neural Basis of Cognition, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8583-4300
  4. 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.
    ORCID icon "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

© 2017, Kanashiro 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.

Metrics

  • 3,559
    views
  • 778
    downloads
  • 75
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Tatjana Kanashiro
  2. Gabriel Koch Ocker
  3. Marlene R Cohen
  4. Brent Doiron
(2017)
Attentional modulation of neuronal variability in circuit models of cortex
eLife 6:e23978.
https://doi.org/10.7554/eLife.23978

Share this article

https://doi.org/10.7554/eLife.23978

Further reading

    1. Neuroscience
    Hannah R Martin, Anna Lysakowski, Ruth Anne Eatock
    Research Article

    In amniotes, head motions and tilt are detected by two types of vestibular hair cells (HCs) with strikingly different morphology and physiology. Mature type I HCs express a large and very unusual potassium conductance, gK,L, which activates negative to resting potential, confers very negative resting potentials and low input resistances, and enhances an unusual non-quantal transmission from type I cells onto their calyceal afferent terminals. Following clues pointing to KV1.8 (Kcna10) in the Shaker K channel family as a candidate gK,L subunit, we compared whole-cell voltage-dependent currents from utricular HCs of KV1.8-null mice and littermate controls. We found that KV1.8 is necessary not just for gK,L but also for fast-inactivating and delayed rectifier currents in type II HCs, which activate positive to resting potential. The distinct properties of the three KV1.8-dependent conductances may reflect different mixing with other KV subunits that are reported to be differentially expressed in type I and II HCs. In KV1.8-null HCs of both types, residual outwardly rectifying conductances include KV7 (Knq) channels. Current clamp records show that in both HC types, KV1.8-dependent conductances increase the speed and damping of voltage responses. Features that speed up vestibular receptor potentials and non-quantal afferent transmission may have helped stabilize locomotion as tetrapods moved from water to land.

    1. Neuroscience
    Yujiro Umezaki, Sergio Hidalgo ... Fumika Hamada
    Research Article

    Hungry animals consistently show a desire to obtain food. Even a brief sensory detection of food can trigger bursts of physiological and behavioral changes. However, the underlying mechanisms by which the sensation of food triggers the acute behavioral response remain elusive. We have previously shown in Drosophila that hunger drives a preference for low temperature. Because Drosophila is a small ectotherm, a preference for low temperature implies a low body temperature and a low metabolic rate. Here, we show that taste-sensing triggers a switch from a low to a high temperature preference in hungry flies. We show that taste stimulation by artificial sweeteners or optogenetics triggers an acute warm preference, but is not sufficient to reach the fed state. Instead, nutrient intake is required to reach the fed state. The data suggest that starvation recovery is controlled by two components: taste-evoked and nutrient-induced warm preferences, and that taste and nutrient quality play distinct roles in starvation recovery. Animals are motivated to eat based on time of day or hunger. We found that clock genes and hunger signals profoundly control the taste-evoked warm preferences. Thus, our data suggest that the taste-evoked response is one of the critical layers of regulatory mechanisms representing internal energy homeostasis and metabolism.