A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity

  1. Naoki Yamawaki
  2. Katharine Borges
  3. Benjamin A Suter
  4. Kenneth D Harris
  5. Gordon M G Shepherd  Is a corresponding author
  1. Northwestern University, United States
  2. University College London, United Kingdom

Abstract

Motor cortex (M1) is classically considered an agranular area, lacking a distinct layer 4 (L4). Here, we tested the idea that M1, despite lacking a cytoarchitecturally visible L4, nevertheless possesses its equivalent in the form of excitatory neurons with input-output circuits like those of L4 neurons in sensory areas. Consistent with this idea, we found that neurons located in a thin laminar zone at the L3/5A border in the forelimb area of mouse M1 have multiple L4-like synaptic connections: excitatory input from thalamus, largely unidirectional excitatory outputs to L2/3 pyramidal neurons, and relatively weak long-range corticocortical inputs and outputs. M1-L4 neurons were electrophysiologically diverse but morphologically uniform, with pyramidal-type dendritic arbors and locally ramifying axons including branches extending into L2/3. Our findings therefore identify pyramidal neurons in M1 with the expected prototypical circuit properties of excitatory L4 neurons, and question the traditional assumption that motor cortex lacks this layer.

Article and author information

Author details

  1. Naoki Yamawaki

    Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Katharine Borges

    Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Benjamin A Suter

    Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kenneth D Harris

    Institute of Neurology, Department of Neuroscience, Physiology, and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Gordon M G Shepherd

    Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    For correspondence
    g-shepherd@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.

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 (1248, 1331, 3310) of Northwestern University.

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Publication history

  1. Received: October 31, 2014
  2. Accepted: December 18, 2014
  3. Accepted Manuscript published: December 19, 2014 (version 1)
  4. Version of Record published: January 14, 2015 (version 2)

Copyright

© 2014, Yamawaki 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. Naoki Yamawaki
  2. Katharine Borges
  3. Benjamin A Suter
  4. Kenneth D Harris
  5. Gordon M G Shepherd
(2014)
A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity
eLife 3:e05422.
https://doi.org/10.7554/eLife.05422

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