Sensory experience inversely regulates feedforward and feedback excitation-inhibition ratio in rodent visual cortex

  1. Nathaniel J Miska
  2. Leonidas MA Richter
  3. Brian A Cary
  4. Julijana Gjorgjieva
  5. Gina G Turrigiano  Is a corresponding author
  1. Brandeis University, United States
  2. Max Planck Institute for Brain Research, Germany

Abstract

Brief (2-3d) monocular deprivation (MD) during the critical period induces a profound loss of responsiveness within binocular (V1b) and monocular (V1m) regions of rodent primary visual cortex. This has largely been ascribed to long-term depression (LTD) at thalamocortical synapses, while a contribution from intracortical inhibition has been controversial. Here we used optogenetics to isolate and measure feedforward thalamocortical and feedback intracortical excitation-inhibition (E-I) ratios following brief MD. Despite depression at thalamocortical synapses, thalamocortical E-I ratio was unaffected in V1b and shifted toward excitation in V1m, indicating that thalamocortical excitation was not effectively reduced. In contrast, feedback intracortical E-I ratio was shifted toward inhibition in V1m, and a computational model demonstrated that these opposing shifts produced an overall suppression of layer 4 excitability. Thus, feedforward and feedback E-I ratios can be independently tuned by visual experience, and enhanced feedback inhibition is the primary driving force behind loss of visual responsiveness.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Individual data points are plotted over bar graphs of means +/- SEM for each figure.

Article and author information

Author details

  1. Nathaniel J Miska

    Department of Biology, 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:" 0000-0001-8587-4919
  2. Leonidas MA Richter

    Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Brian A Cary

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Julijana Gjorgjieva

    Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7118-4079
  5. Gina G Turrigiano

    Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    turrigiano@brandeis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4476-4059

Funding

National Science Foundation (NSF10604)

  • Nathaniel J Miska

National Institute of Neurological Disorders and Stroke (F31 NS089170)

  • Nathaniel J Miska

National Eye Institute (R01 EY025613)

  • Gina G Turrigiano

Max-Planck-Gesellschaft

  • Julijana Gjorgjieva

National Institute of Neurological Disorders and Stroke (R37 NS092635)

  • Gina G Turrigiano

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 Brandeis University institutional animal care and use committee (IACUC) protocols (#15005 and #18002). All surgery was performed under ketamine-xylazine-acepromazine anesthesia and included sufficient post-operative analgesia to minimize any animal suffering.

Reviewing Editor

  1. Julie A Kauer, Brown University, United States

Publication history

  1. Received: June 1, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 12, 2018 (version 1)
  4. Version of Record published: November 8, 2018 (version 2)

Copyright

© 2018, Miska 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

  • 3,663
    Page views
  • 606
    Downloads
  • 26
    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. Nathaniel J Miska
  2. Leonidas MA Richter
  3. Brian A Cary
  4. Julijana Gjorgjieva
  5. Gina G Turrigiano
(2018)
Sensory experience inversely regulates feedforward and feedback excitation-inhibition ratio in rodent visual cortex
eLife 7:e38846.
https://doi.org/10.7554/eLife.38846

Further reading

    1. Neuroscience
    Liqiang Chen et al.
    Short Report

    The presynaptic protein α-synuclein (αSyn) has been suggested to be involved in the pathogenesis of Parkinson’s disease (PD). In PD, the amygdala is prone to develop insoluble αSyn aggregates, and it has been suggested that circuit dysfunction involving the amygdala contributes to the psychiatric symptoms. Yet, how αSyn aggregates affect amygdala function is unknown. In this study, we examined αSyn in glutamatergic axon terminals and the impact of its aggregation on glutamatergic transmission in the basolateral amygdala (BLA). We found that αSyn is primarily present in the vesicular glutamate transporter 1-expressing (vGluT1+) terminals in mouse BLA, which is consistent with higher levels of αSyn expression in vGluT1+ glutamatergic neurons in the cerebral cortex relative to the vGluT2+ glutamatergic neurons in the thalamus. We found that αSyn aggregation selectively decreased the cortico-BLA, but not the thalamo-BLA, transmission; and that cortico-BLA synapses displayed enhanced short-term depression upon repetitive stimulation. In addition, using confocal microscopy, we found that vGluT1+ axon terminals exhibited decreased levels of soluble αSyn, which suggests that lower levels of soluble αSyn might underlie the enhanced short-term depression of cortico-BLA synapses. In agreement with this idea, we found that cortico-BLA synaptic depression was also enhanced in αSyn knockout mice. In conclusion, both basal and dynamic cortico-BLA transmission were disrupted by abnormal aggregation of αSyn and these changes might be relevant to the perturbed cortical control of the amygdala that has been suggested to play a role in psychiatric symptoms in PD.

    1. Evolutionary Biology
    2. Neuroscience
    Elias T Lunsford et al.
    Research Article Updated

    Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.