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Research Article

Subplate neurons are the first cortical neurons to respond to sensory stimuli

Jessica M. Wess, Amal Isaiah, Paul V. Watkins, and View ORCID ProfilePatrick O. Kanold
PNAS November 21, 2017 114 (47) 12602-12607; first published November 7, 2017; https://doi.org/10.1073/pnas.1710793114
Jessica M. Wess
aDepartment of Biology, University of Maryland, College Park, MD 20742;
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Amal Isaiah
aDepartment of Biology, University of Maryland, College Park, MD 20742;
bDepartment of Otorhinolaryngology—Head and Neck Surgery, University of Maryland, Baltimore, MD 21201
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Paul V. Watkins
aDepartment of Biology, University of Maryland, College Park, MD 20742;
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Patrick O. Kanold
aDepartment of Biology, University of Maryland, College Park, MD 20742;
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  • ORCID record for Patrick O. Kanold
  • For correspondence: pkanold@umd.edu
  1. Edited by Carla J. Shatz, Stanford University, Stanford, CA, and approved October 19, 2017 (received for review June 14, 2017)

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Significance

Sensory experience, even at prenatal periods, can shape brain connectivity. Thus, the emergence of sensory responses is a key step in cortical development. Sensory cortical responses are thought to emerge in cortical layer 4, which is the adult target of thalamic projections. However, in developing animals, thalamic fibers do not target layer 4 but instead target subplate neurons in the white matter. We show that subplate neurons respond to sounds before layer 4 is activated by thalamic axons. Moreover, early local field potential (LFP) responses demonstrate nascent topographic organization. Together we find that sound-evoked cortical activity and topographic organization emerge in a different layer than thought. Since subplate circuits are disrupted in autism spectrum disorder (ASD) models, disrupted emergence of sensory activity could be utilized for diagnosis and intervention.

Abstract

In utero experience, such as maternal speech in humans, can shape later perception, although the underlying cortical substrate is unknown. In adult mammals, ascending thalamocortical projections target layer 4, and the onset of sensory responses in the cortex is thought to be dependent on the onset of thalamocortical transmission to layer 4 as well as the ear and eye opening. In developing animals, thalamic fibers do not target layer 4 but instead target subplate neurons deep in the developing white matter. We investigated if subplate neurons respond to sensory stimuli. Using electrophysiological recordings in young ferrets, we show that auditory cortex neurons respond to sound at very young ages, even before the opening of the ears. Single unit recordings showed that auditory responses emerged first in cortical subplate neurons. Subsequently, responses appeared in the future thalamocortical input layer 4, and sound-evoked spike latencies were longer in layer 4 than in subplate, consistent with the known relay of thalamic information to layer 4 by subplate neurons. Electrode array recordings show that early auditory responses demonstrate a nascent topographic organization, suggesting that topographic maps emerge before the onset of spiking responses in layer 4. Together our results show that sound-evoked activity and topographic organization of the cortex emerge earlier and in a different layer than previously thought. Thus, early sound experience can activate and potentially sculpt subplate circuits before permanent thalamocortical circuits to layer 4 are present, and disruption of this early sensory activity could be utilized for early diagnosis of developmental disorders.

  • cortex
  • development
  • fetal
  • hearing
  • sensory

Footnotes

  • ↵1J.M.W. and A.I. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: pkanold{at}umd.edu.
  • Author contributions: P.O.K. designed research; J.M.W. performed research; J.M.W., A.I., P.V.W., and P.O.K. analyzed data; and P.O.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1710793114/-/DCSupplemental.

Published under the PNAS license.

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Sensory cortical responses emerge in the subplate
Jessica M. Wess, Amal Isaiah, Paul V. Watkins, Patrick O. Kanold
Proceedings of the National Academy of Sciences Nov 2017, 114 (47) 12602-12607; DOI: 10.1073/pnas.1710793114

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Sensory cortical responses emerge in the subplate
Jessica M. Wess, Amal Isaiah, Paul V. Watkins, Patrick O. Kanold
Proceedings of the National Academy of Sciences Nov 2017, 114 (47) 12602-12607; DOI: 10.1073/pnas.1710793114
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