Developmental 'awakening' of primary motor cortex to the sensory consequences of movement

  1. James C Dooley  Is a corresponding author
  2. Mark S Blumberg
  1. University of Iowa, United States

Abstract

Before primary motor cortex (M1) develops its motor functions, it functions like a somatosensory area. Here, by recording from neurons in the forelimb representation of M1 in postnatal day (P) 8-12 rats, we demonstrate a rapid shift in its sensory responses. At P8-10, M1 neurons respond overwhelmingly to feedback from sleep-related twitches of the forelimb, but the same neurons do not respond to wake-related movements. By P12, M1 neurons suddenly respond to wake movements, a transition that results from opening the sensory gate in the external cuneate nucleus. Also at P12, fewer M1 neurons respond to individual twitches, but the full complement of twitch-related feedback observed at P8 is unmasked through local disinhibition. Finally, through P12, M1 sensory responses originate in the deep thalamorecipient layers, not primary somatosensory cortex. These findings demonstrate that M1 initially establishes a sensory framework upon which its later-emerging role in motor control is built.

Data availability

Data represented in all figures is summarized in the included tables. Because of the large amount of data in the present publication (over 1,000 neurons across over 50 animals, along with thousands of behaviorally scored twitches and wake movements) our raw data (neural firing timecodes and behavioral event timecodes) have been uploaded to Dryad at DOI: https://doi.org/10.5061/dryad.8231nj1. Custom MATLAB scripts for generating and fitting perievent histograms to twitch and wake movement models can be found on github (https://github.com/jcdooley/Dooley_and_Blumberg_2018).

The following data sets were generated
    1. Dooley J
    2. Blumberg M
    (2018) Data from: Developmental
    Dryad Digital Repository, doi:10.5061/dryad.8231nj1.

Article and author information

Author details

  1. James C Dooley

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    For correspondence
    james-c-dooley@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9868-9840
  2. Mark S Blumberg

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6969-2955

Funding

National Institutes of Health (R37-HD081168)

  • Mark S Blumberg

National Institutes of Health (F32-NS101858)

  • James C Dooley

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were conducted in accordance with the National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals (NIH Publication No. 80-23) and were approved by the Institutional Animal Care and Use Committee of the University of Iowa (protocol # 7011955).

Copyright

© 2018, Dooley & Blumberg

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

  • 4,771
    views
  • 490
    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. James C Dooley
  2. Mark S Blumberg
(2018)
Developmental 'awakening' of primary motor cortex to the sensory consequences of movement
eLife 7:e41841.
https://doi.org/10.7554/eLife.41841

Share this article

https://doi.org/10.7554/eLife.41841

Further reading

    1. Neuroscience
    Magdalena Ziółkowska, Narges Sotoudeh ... Kasia Radwanska
    Research Article

    The ability to extinguish contextual fear in a changing environment is crucial for animal survival. Recent data support the role of the thalamic nucleus reuniens (RE) and its projections to the dorsal hippocampal CA1 area (RE→dCA1) in this process. However, it remains poorly understood how RE impacts dCA1 neurons during contextual fear extinction (CFE). Here, we reveal that the RE→dCA1 pathway contributes to the extinction of contextual fear by affecting CFE-induced molecular remodeling of excitatory synapses. Anatomical tracing and chemogenetic manipulation in mice demonstrate that RE neurons form synapses and regulate synaptic transmission in the stratum oriens (SO) and lacunosum-moleculare (SLM) of the dCA1 area, but not in the stratum radiatum (SR). We also observe CFE-specific structural changes of excitatory synapses and expression of the synaptic scaffold protein, PSD-95, in both strata innervated by RE, but not in SR. Interestingly, only the changes in SLM are specific for the dendrites innervated by RE. To further support the role of the RE→dCA1 projection in CFE, we demonstrate that brief chemogenetic inhibition of the RE→dCA1 pathway during a CFE session persistently impairs the formation of CFE memory and CFE-induced changes of PSD-95 levels in SLM. Thus, our data indicate that RE participates in CFE by regulating CFE-induced molecular remodeling of dCA1 synapses.

    1. Computational and Systems Biology
    2. Neuroscience
    Cesare V Parise, Marc O Ernst
    Research Article

    Audiovisual information reaches the brain via both sustained and transient input channels, representing signals’ intensity over time or changes thereof, respectively. To date, it is unclear to what extent transient and sustained input channels contribute to the combined percept obtained through multisensory integration. Based on the results of two novel psychophysical experiments, here we demonstrate the importance of the transient (instead of the sustained) channel for the integration of audiovisual signals. To account for the present results, we developed a biologically inspired, general-purpose model for multisensory integration, the multisensory correlation detectors, which combines correlated input from unimodal transient channels. Besides accounting for the results of our psychophysical experiments, this model could quantitatively replicate several recent findings in multisensory research, as tested against a large collection of published datasets. In particular, the model could simultaneously account for the perceived timing of audiovisual events, multisensory facilitation in detection tasks, causality judgments, and optimal integration. This study demonstrates that several phenomena in multisensory research that were previously considered unrelated, all stem from the integration of correlated input from unimodal transient channels.