Multiple regions of sensorimotor cortex encode bite force and gape
The precise control of bite force and gape is vital for safe and 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...
Main Authors: | , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2023-09-01
|
Series: | Frontiers in Systems Neuroscience |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fnsys.2023.1213279/full |
_version_ | 1797677647859286016 |
---|---|
author | Fritzie I. Arce-McShane Fritzie I. Arce-McShane Barry J. Sessle Yasheshvini Ram Callum F. Ross Nicholas G. Hatsopoulos |
author_facet | Fritzie I. Arce-McShane Fritzie I. Arce-McShane Barry J. Sessle Yasheshvini Ram Callum F. Ross Nicholas G. Hatsopoulos |
author_sort | Fritzie I. Arce-McShane |
collection | DOAJ |
description | The precise control of bite force and gape is vital for safe and 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 static 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 vs. 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 static gape during biting 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. |
first_indexed | 2024-03-11T22:48:18Z |
format | Article |
id | doaj.art-ecc723fcdec344ff83dea025b384f988 |
institution | Directory Open Access Journal |
issn | 1662-5137 |
language | English |
last_indexed | 2024-03-11T22:48:18Z |
publishDate | 2023-09-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Systems Neuroscience |
spelling | doaj.art-ecc723fcdec344ff83dea025b384f9882023-09-22T07:53:03ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372023-09-011710.3389/fnsys.2023.12132791213279Multiple regions of sensorimotor cortex encode bite force and gapeFritzie I. Arce-McShane0Fritzie I. Arce-McShane1Barry J. Sessle2Yasheshvini Ram3Callum F. Ross4Nicholas G. Hatsopoulos5Department of Oral Health Sciences, School of Dentistry, University of Washington, Seattle, WA, United StatesGraduate Program in Neuroscience, University of Washington, Seattle, WA, United StatesFaculty of Dentistry and Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, ON, CanadaDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, United StatesDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, United StatesDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, United StatesThe precise control of bite force and gape is vital for safe and 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 static 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 vs. 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 static gape during biting 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.https://www.frontiersin.org/articles/10.3389/fnsys.2023.1213279/fullsensorimotor cortexforcegapeencodingdecompositionpopulation activity |
spellingShingle | Fritzie I. Arce-McShane Fritzie I. Arce-McShane Barry J. Sessle Yasheshvini Ram Callum F. Ross Nicholas G. Hatsopoulos Multiple regions of sensorimotor cortex encode bite force and gape Frontiers in Systems Neuroscience sensorimotor cortex force gape encoding decomposition population activity |
title | Multiple regions of sensorimotor cortex encode bite force and gape |
title_full | Multiple regions of sensorimotor cortex encode bite force and gape |
title_fullStr | Multiple regions of sensorimotor cortex encode bite force and gape |
title_full_unstemmed | Multiple regions of sensorimotor cortex encode bite force and gape |
title_short | Multiple regions of sensorimotor cortex encode bite force and gape |
title_sort | multiple regions of sensorimotor cortex encode bite force and gape |
topic | sensorimotor cortex force gape encoding decomposition population activity |
url | https://www.frontiersin.org/articles/10.3389/fnsys.2023.1213279/full |
work_keys_str_mv | AT fritzieiarcemcshane multipleregionsofsensorimotorcortexencodebiteforceandgape AT fritzieiarcemcshane multipleregionsofsensorimotorcortexencodebiteforceandgape AT barryjsessle multipleregionsofsensorimotorcortexencodebiteforceandgape AT yasheshviniram multipleregionsofsensorimotorcortexencodebiteforceandgape AT callumfross multipleregionsofsensorimotorcortexencodebiteforceandgape AT nicholasghatsopoulos multipleregionsofsensorimotorcortexencodebiteforceandgape |