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Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape

View ORCID ProfileFritzie I. Arce-McShane, Barry J. Sessle, Yasheshvini Ram, Carrie A. Balcer, Callum F. Ross, Nicholas G. Hatsopoulos
doi: https://doi.org/10.1101/2020.08.16.252817
Fritzie I. Arce-McShane
1Department of Organismal Biology and Anatomy, University of Chicago, 1027 E 57th Street, Chicago, IL 60637
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  • ORCID record for Fritzie I. Arce-McShane
  • For correspondence: fritziea@uchicago.edu
Barry J. Sessle
2Faculty of Dentistry, and Department of Physiology, Faculty of Medicine, University of Toronto, 124 Edward Street, Toronto, Ontario M5G 1G6, CANADA
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Yasheshvini Ram
1Department of Organismal Biology and Anatomy, University of Chicago, 1027 E 57th Street, Chicago, IL 60637
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Carrie A. Balcer
1Department of Organismal Biology and Anatomy, University of Chicago, 1027 E 57th Street, Chicago, IL 60637
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Callum F. Ross
1Department of Organismal Biology and Anatomy, University of Chicago, 1027 E 57th Street, Chicago, IL 60637
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Nicholas G. Hatsopoulos
1Department of Organismal Biology and Anatomy, University of Chicago, 1027 E 57th Street, Chicago, IL 60637
3Committees on Computational Neuroscience and Neurobiology, University of Chicago
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Abstract

The precise control of bite force and gape is vital for effective breakdown and manipulation of food inside the oral cavity during feeding. Yet the role of the orofacial sensorimotor cortex (OSMcx) in the control of bite force and gape is still largely unknown. The aim of this study was to elucidate how individual neurons and populations of neurons in multiple regions of OSMcx differentially encode bite force and gape when subjects (Macaca mulatta) generated different levels of bite force at varying gapes. We examined neuronal activity recorded simultaneously from three microelectrode arrays implanted chronically in the primary motor (MIo), primary somatosensory (SIo), and cortical masticatory (CMA) areas of OSMcx. We used generalized linear models to evaluate encoding properties of individual neurons and utilized dimensionality reduction techniques to decompose population activity into components related to specific task parameters. Individual neurons encoded bite force more strongly than gape in all three OSMCx areas although bite force was a better predictor of spiking activity in MIo versus SIo. Population activity differentiated between levels of bite force and gape while preserving task-independent temporal modulation across the behavioral trial. While activation patterns of neuronal populations were comparable across OSMCx areas, the total variance explained by task parameters was context-dependent and differed across areas. These findings suggest that the cortical control of gape may rely on computations at the population level whereas the strong encoding of bite force at the individual neuron level allows for the precise and rapid control of bite force.

Significance Statement Biting a piece off an apple requires precise sensorimotor control and coordination of bite force and gape by multiple brain regions. The cortical representations of bite force and gape by individual neurons and large populations of neurons across connected motor and somatosensory areas in orofacial cortex is unknown. Here we showed that bite force was more strongly encoded than gape by individual neurons in primary motor, somatosensory, and cortical masticatory areas. Moreover, bite force was more effectively represented in motor versus somatosensory cortices. At the population level, bite force and gape were distinguishable particularly when gape was randomized from trial-to-trial. The results are important for understanding neurophysiological processes underlying masticatory dysfunctions that may occur in aging, stroke, and Alzheimer’s disease.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵**Co-senior authors

  • Acknowledgment; improved format of figures with text

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted August 17, 2020.
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Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape
Fritzie I. Arce-McShane, Barry J. Sessle, Yasheshvini Ram, Carrie A. Balcer, Callum F. Ross, Nicholas G. Hatsopoulos
bioRxiv 2020.08.16.252817; doi: https://doi.org/10.1101/2020.08.16.252817
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Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape
Fritzie I. Arce-McShane, Barry J. Sessle, Yasheshvini Ram, Carrie A. Balcer, Callum F. Ross, Nicholas G. Hatsopoulos
bioRxiv 2020.08.16.252817; doi: https://doi.org/10.1101/2020.08.16.252817

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