Cell type specific control of basolateral amygdala neuronal circuits via entorhinal cortex-driven feedforward inhibition

  1. E Mae Guthman
  2. Joshua D Garcia
  3. Ming Ma
  4. Philip Chu
  5. Serapio M Baca
  6. Katharine R Smith
  7. Diego Restrepo
  8. Molly M Huntsman  Is a corresponding author
  1. University of Colorado Anschutz Medical Campus, United States

Abstract

The basolateral amygdala (BLA) plays a vital role in associating sensory stimuli with salient valence information. Excitatory principal neurons (PNs) undergo plastic changes to encode this association; however, local BLA inhibitory interneurons (INs) gate PN plasticity via feedforward inhibition (FFI). Despite literature implicating parvalbumin expressing (PV+) INs in FFI in cortex and hippocampus, prior anatomical experiments in BLA implicate somatostatin expressing (Sst+) INs. The lateral entorhinal cortex (LEC) projects to BLA where it drives FFI. In the present study, we explored the role of interneurons in this circuit. Using mice, we combined patch clamp electrophysiology, chemogenetics, unsupervised cluster analysis, and predictive modeling and found that a previously unreported subpopulation of fast-spiking Sst+ INs mediate LEC→BLA FFI.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. E Mae Guthman

    Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2190-7520
  2. Joshua D Garcia

    Department of Pharmacology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ming Ma

    Department of Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Philip Chu

    Department of Pharmaceutical Sciences, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Serapio M Baca

    Department of Pharmaceutical Sciences, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Katharine R Smith

    Department of Pharmacology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Diego Restrepo

    Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4972-446X
  8. Molly M Huntsman

    Department of Pharmaceutical Sciences, University of Colorado Anschutz Medical Campus, Aurora, United States
    For correspondence
    molly.huntsman@CUAnschutz.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5954-0023

Funding

National Institutes of Health (NS095311)

  • Molly M Huntsman

National Science Foundation (DGE-1553798)

  • E Mae Guthman

National Institutes of Health (DC000566)

  • Diego Restrepo

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 the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#00039) of the University of Colorado Denver | Anschutz Medical Campus.

Reviewing Editor

  1. John Huguenard, Stanford University School of Medicine, United States

Publication history

  1. Received: July 27, 2019
  2. Accepted: January 8, 2020
  3. Accepted Manuscript published: January 9, 2020 (version 1)
  4. Version of Record published: January 27, 2020 (version 2)

Copyright

© 2020, Guthman 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.

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  1. E Mae Guthman
  2. Joshua D Garcia
  3. Ming Ma
  4. Philip Chu
  5. Serapio M Baca
  6. Katharine R Smith
  7. Diego Restrepo
  8. Molly M Huntsman
(2020)
Cell type specific control of basolateral amygdala neuronal circuits via entorhinal cortex-driven feedforward inhibition
eLife 9:e50601.
https://doi.org/10.7554/eLife.50601

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