Neural coding in barrel cortex during whisker-guided locomotion

  1. Nicholas James Sofroniew
  2. Yurii A Vlasov
  3. Samuel Andrew Hires
  4. Jeremy Freeman
  5. Karel Svoboda  Is a corresponding author
  1. Janelia Research Center, Howard Hughes Medical Institute, United States
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
  3. University of Southern California, United States

Abstract

Animals seek out relevant information by moving through a dynamic world, but sensory systems are usually studied under highly constrained and passive conditions that may not probe important dimensions of the neural code. Here we explored neural coding in the barrel cortex of head-fixed mice that tracked walls with their whiskers in tactile virtual reality. Optogenetic manipulations revealed that barrel cortex plays a role in wall-tracking. Closed-loop optogenetic control of layer 4 neurons can substitute for whisker-object contact to guide behavior resembling wall tracking. We measured neural activity using two-photon calcium imaging and extracellular recordings. Neurons were tuned to the distance between the animal snout and the contralateral wall, with monotonic, unimodal, and multimodal tuning curves. This rich representation of object location in the barrel cortex could not be predicted based on simple stimulus-response relationships involving individual whiskers and likely emerges within cortical circuits.

Article and author information

Author details

  1. Nicholas James Sofroniew

    Janelia Research Center, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yurii A Vlasov

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Samuel Andrew Hires

    Biological Sciences, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jeremy Freeman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Karel Svoboda

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    svobodak@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures were in accordance with protocols approved by the Janelia Institutional Animal Care and Use Committee. (IACUC 14-115)

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Publication history

  1. Received: October 24, 2015
  2. Accepted: December 21, 2015
  3. Accepted Manuscript published: December 23, 2015 (version 1)
  4. Version of Record published: February 11, 2016 (version 2)

Copyright

© 2015, Sofroniew 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

  • 6,186
    Page views
  • 1,377
    Downloads
  • 64
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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. Nicholas James Sofroniew
  2. Yurii A Vlasov
  3. Samuel Andrew Hires
  4. Jeremy Freeman
  5. Karel Svoboda
(2015)
Neural coding in barrel cortex during whisker-guided locomotion
eLife 4:e12559.
https://doi.org/10.7554/eLife.12559
  1. Further reading

Further reading

    1. Neuroscience
    Na Young Jun, Douglas A Ruff ... Jennifer M Groh
    Research Article

    Sensory receptive fields are large enough that they can contain more than one perceptible stimulus. How, then, can the brain encode information about each of the stimuli that may be present at a given moment? We recently showed that when more than one stimulus is present, single neurons can fluctuate between coding one vs. the other(s) across some time period, suggesting a form of neural multiplexing of different stimuli (Caruso et al., 2018). Here, we investigate (a) whether such coding fluctuations occur in early visual cortical areas; (b) how coding fluctuations are coordinated across the neural population; and (c) how coordinated coding fluctuations depend on the parsing of stimuli into separate vs. fused objects. We found coding fluctuations do occur in macaque V1 but only when the two stimuli form separate objects. Such separate objects evoked a novel pattern of V1 spike count (‘noise’) correlations involving distinct distributions of positive and negative values. This bimodal correlation pattern was most pronounced among pairs of neurons showing the strongest evidence for coding fluctuations or multiplexing. Whether a given pair of neurons exhibited positive or negative correlations depended on whether the two neurons both responded better to the same object or had different object preferences. Distinct distributions of spike count correlations based on stimulus preferences were also seen in V4 for separate objects but not when two stimuli fused to form one object. These findings suggest multiple objects evoke different response dynamics than those evoked by single stimuli, lending support to the multiplexing hypothesis and suggesting a means by which information about multiple objects can be preserved despite the apparent coarseness of sensory coding.

    1. Neuroscience
    Sebastian GW Urchs, Angela Tam ... Pierre Bellec
    Research Article

    Our understanding of the changes in functional brain organization in autism is hampered by the extensive heterogeneity that characterizes this neurodevelopmental disorder. Data driven clustering offers a straightforward way to decompose autism heterogeneity into subtypes of connectivity and promises an unbiased framework to investigate behavioral symptoms and causative genetic factors. Yet, the robustness and generalizability of functional connectivity subtypes is unknown. Here, we show that a simple hierarchical cluster analysis can robustly relate a given individual and brain network to a connectivity subtype, but that continuous assignments are more robust than discrete ones. We also found that functional connectivity subtypes are moderately associated with the clinical diagnosis of autism, and these associations generalize to independent replication data. We explored systematically 18 different brain networks as we expected them to associate with different behavioral profiles as well as different key regions. Contrary to this prediction, autism functional connectivity subtypes converged on a common topography across different networks, consistent with a compression of the primary gradient of functional brain organization, as previously reported in the literature. Our results support the use of data driven clustering as a reliable data dimensionality reduction technique, where any given dimension only associates moderately with clinical manifestations.