Cited by 213Neuroscience and Music PerceptionHearing, Cochlea, Tinnitus, GeneticsMultisensory perception and integration

A circuit for motor cortical modulation of auditory cortical activity

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Nelson, Anders, Schneider, David M., Takatoh, Jun, Sakurai, Katsuyasu, Wang, Fan, Mooney, Richard·2013·The Journal of Neuroscience

Abstract

Normal hearing depends on the ability to distinguish self-generated sounds from other sounds, and this ability is thought to involve neural circuits that convey copies of motor command signals to various levels of the auditory system. Although such interactions at the cortical level are believed to facilitate auditory comprehension during movements and drive auditory hallucinations in pathological states, the synaptic organization and function of circuitry linking the motor and auditory cortices remain unclear. Here we describe experiments in the mouse that characterize circuitry well suited to transmit motor-related signals to the auditory cortex. Using retrograde viral tracing, we established that neurons in superficial and deep layers of the medial agranular motor cortex (M2) project directly to the auditory cortex and that the axons of some of these deep-layer cells also target brainstem motor regions. Using in vitro whole-cell physiology, optogenetics, and pharmacology, we determined that M2 axons make excitatory synapses in the auditory cortex but exert a primarily suppressive effect on auditory cortical neuron activity mediated in part by feedforward inhibition involving parvalbumin-positive interneurons. Using in vivo intracellular physiology, optogenetics, and sound playback, we also found that directly activating M2 axon terminals in the auditory cortex suppresses spontaneous and stimulus-evoked synaptic activity in auditory cortical neurons and that this effect depends on the relative timing of motor cortical activity and auditory stimulation. These experiments delineate the structural and functional properties of a corticocortical circuit that could enable movement-related suppression of auditory cortical activity.

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Crossref · 10.1523/jneurosci.2275-13.2013

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  • Only a subset of motor cortical neurons projecting to auditory cortex modulate their discharge in relation to locomotion under head fixation.

    “For example, only a subset of motor cortical neurons that project to auditory cortex modulate their discharge in relation to locomotion under head fixation”

    From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Nelson et al., 2013

  • Recent studies have identified thalamocortical, corticocortical and corticothalamic pathways that can control cortical state and sensory responsiveness with high temporal and spatial specificity.

    “In addition to the modulation of cortical neuronal excitability by ascending noradrenergic and cholinergic systems, recent studies have identified thalamocortical, corticocortical and corticothalamic pathways that can control cortical state and sensory responsiveness with high temporal and spatial specificity, owing to their activation of ionotropic and metabotropic glutamate receptors (Nelson et”

    From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Nelson et al., 2013

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Authors
Nelson, A., Schneider, D. M., Takatoh, J., Sakurai, K., Wang, F., & Mooney, R.
Affiliations
Duke Medical Center (US)
Venue
The Journal of Neuroscience
Published
2013-09-04
Volume
33
Issue
36
Pages
14342-14353
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W1970177188
Cited by
213
References
76
Citations by year
2026: 12 · 2025: 10 · 2024: 23 · 2023: 12 · 2022: 17 · 2021: 18 · 2020: 20 · 2019: 37 · 2018: 13 · 2017: 15 · 2016: 17 · 2015: 8 · 2014: 11
FWCI
6.56
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Institute on Drug Abuse (DA028302, R01DA028302)
  • National Institute on Deafness and Other Communication Disorders (F31DC013976)
  • National Institute of General Medical Sciences (T32GM008441)
  • National Institute of Neurological Disorders and Stroke (NS 077986, R01NS077986, NS079929, R21NS079929)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
  • Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Keywords
motor cortex, auditory cortex, M2, feedforward inhibition, parvalbumin interneurons, auditory hallucinations
MeSH terms
Action Potentials, Animals, Auditory Cortex, Axons, Brain Stem, Interneurons, Mice, Inbred C57BL, Motor Cortex, Motor Neurons, Nerve Net, Synapses, Pyramidal Cells, Feedback, Physiological, Mice, Synaptic Potentials

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