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

  1. Narendra Mukherjee
  2. Joseph Wachutka
  3. Donald B Katz  Is a corresponding author
  1. Brandeis University, United States

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.

Data availability

We have structured our electrophysiology datasets in a hierarchical data format (HDF5) and are hosting the files on a university-wide network share managed by Library and Technology Services (LTS) at Brandeis University. These HDF5 files contain our electrophysiology recordings, sorted spikes, single-neuron and population-level analyses (and associated plots and results). These files are prohibitively large to be hosted on a general-purpose fileshare platform - we request anyone interested in our datasets to contact the corresponding author, Donald Katz (dbkatz@brandeis.edu) who can put them in touch with LTS in order to create a guest account at Brandeis through which they can securely access our datasets (hosted on the katz-lab share at files.brandeis.edu).

Article and author information

Author details

  1. Narendra Mukherjee

    Program in Neuroscience, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3808-2622
  2. Joseph Wachutka

    Program in Neuroscience, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.
    ORCID icon "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.

Copyright

© 2019, Mukherjee 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

  • 2,047
    views
  • 254
    downloads
  • 50
    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. Narendra Mukherjee
  2. Joseph Wachutka
  3. Donald B Katz
(2019)
Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics
eLife 8:e45968.
https://doi.org/10.7554/eLife.45968

Share this article

https://doi.org/10.7554/eLife.45968

Further reading

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.