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Cover ArticleResearch Articles, Systems/Circuits

Interareal Synaptic Inputs Underlying Whisking-Related Activity in the Primary Somatosensory Barrel Cortex

Masahiro Kawatani, Kayo Horio, Mahito Ohkuma, Wan-Ru Li and Takayuki Yamashita
Journal of Neuroscience 24 January 2024, 44 (4) e1148232023; https://doi.org/10.1523/JNEUROSCI.1148-23.2023
Masahiro Kawatani
1Department of Physiology, Fujita Health University School of Medicine, Toyoake, 470-1192, Japan
2Department of Functional Anatomy and Neuroscience, Graduate School of Medicine, Nagoya University, Nagoya, 466-8550, Japan
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Kayo Horio
1Department of Physiology, Fujita Health University School of Medicine, Toyoake, 470-1192, Japan
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Mahito Ohkuma
1Department of Physiology, Fujita Health University School of Medicine, Toyoake, 470-1192, Japan
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Wan-Ru Li
1Department of Physiology, Fujita Health University School of Medicine, Toyoake, 470-1192, Japan
2Department of Functional Anatomy and Neuroscience, Graduate School of Medicine, Nagoya University, Nagoya, 466-8550, Japan
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Takayuki Yamashita
1Department of Physiology, Fujita Health University School of Medicine, Toyoake, 470-1192, Japan
3International Center for Brain Science (ICBS), Fujita Health University, Toyoake, 470-1192, Japan
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Abstract

Body movements influence brain-wide neuronal activities. In the sensory cortex, thalamocortical bottom-up inputs and motor-sensory top-down inputs are thought to affect the dynamics of membrane potentials (Vm) of neurons and change their processing of sensory information during movements. However, direct perturbation of the axons projecting to the sensory cortex from other remote areas during movements has remained unassessed, and therefore the interareal circuits generating motor-related signals in sensory cortices remain unclear. Using a Gi/o-coupled opsin, eOPN3, we here inhibited interareal signals incoming to the whisker primary somatosensory barrel cortex (wS1) of awake male mice and tested their effects on whisking-related changes in neuronal activities in wS1. Spontaneous whisking in air induced the changes in spike rates of a subset of wS1 neurons, which were accompanied by depolarization and substantial reduction of slow-wave oscillatory fluctuations of Vm. Despite an extensive innervation, inhibition of inputs from the whisker primary motor cortex (wM1) to wS1 did not alter the spike rates and Vm dynamics of wS1 neurons during whisking. In contrast, inhibition of axons from the whisker-related thalamus (wTLM) and the whisker secondary somatosensory cortex (wS2) to wS1 largely attenuated the whisking-related supra- and sub-threshold Vm dynamics of wS1 neurons. Notably, silencing inputs from wTLM markedly decreased the modulation depth of whisking phase-tuned neurons in wS1, while inhibiting wS2 inputs did not impact the whisking variable tuning of wS1 neurons. Thus, sensorimotor integration in wS1 during spontaneous whisking is predominantly facilitated by direct synaptic inputs from wTLM and wS2 rather than from wM1.

  • eOPN3
  • motor cortex
  • sensorimotor integration
  • somatosensory cortex
  • thalamus
  • whisker

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 44 (4)
Journal of Neuroscience
Vol. 44, Issue 4
24 Jan 2024
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Interareal Synaptic Inputs Underlying Whisking-Related Activity in the Primary Somatosensory Barrel Cortex
Masahiro Kawatani, Kayo Horio, Mahito Ohkuma, Wan-Ru Li, Takayuki Yamashita
Journal of Neuroscience 24 January 2024, 44 (4) e1148232023; DOI: 10.1523/JNEUROSCI.1148-23.2023

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Interareal Synaptic Inputs Underlying Whisking-Related Activity in the Primary Somatosensory Barrel Cortex
Masahiro Kawatani, Kayo Horio, Mahito Ohkuma, Wan-Ru Li, Takayuki Yamashita
Journal of Neuroscience 24 January 2024, 44 (4) e1148232023; DOI: 10.1523/JNEUROSCI.1148-23.2023
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Keywords

  • eOPN3
  • motor cortex
  • sensorimotor integration
  • somatosensory cortex
  • thalamus
  • whisker

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