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

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 StatementBiting 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.

Impact of volume and rate of milk delivery on coordination of respiration and swallowing in infant pigs

“…Feeding itself is made of a sequence of behaviors including oral processing (chewing) and pharyngeal swallow that move the bolus through a series of continuous anatomical spaces (Hiiemae & Crompton, 1985). The neurological control of oral and pharyngeal phases of feeding is distinct (Arce‐McShane et al, 2020; Jean, 2001; Moore et al, 2014), yet sensorimotor information from the oral stage of feeding can modify characteristics of the pharyngeal swallow in several ways. Hyoid movements match expectations of motor learning (feedforward loops) only when food is delivered to the oral cavity (Humbert et al, 2012).…”

“…The neurological control of oral and pharyngeal phases of feeding is distinct (Arce-McShane et al, 2020;Jean, 2001;Moore et al, 2014), yet sensorimotor information from the oral stage of feeding can modify characteristics of the pharyngeal swallow in several ways.…”

Multiple regions of sensorimotor cortex encode bite force and gape

“…For example, ICMS in MIo, SIo, or CMA can evoke relatively simple movements of orofacial muscles (e.g., jaw opening, tongue protrusion) as well as more complex movements such as chewing and swallowing (Huang et al, 1988 , 1989b ; Martin et al, 1997 , 1999 ; Hatanaka et al, 2005 ; Laurence-Chasen et al, 2018 ). Neurons in MIo and SIo have been shown to modulate their activity during feeding and performance of orofacial tasks such as the generation of tongue-protrusive force or bite force, to encode the direction and magnitude of tongue-protrusive force, to form coherent networks within and across these areas in a reciprocal manner, and to undergo learning-induced plasticity (Murray and Sessle, 1992a , b ; Lin et al, 1994 ; Arce et al, 2013 ; Arce-McShane et al, 2016 , 2019 ; Liu et al, 2019 ). Many of these neurons have orofacial mechanosensitive RFs and the sensory inputs from their RFs are used to modulate bite and tongue forces (Huang et al, 1988 , 1989b ; Lin and Sessle, 1994 ; Toda and Taoka, 2002 , 2004 ; Cerkevich et al, 2014 ).…”