Unilateral lingual nerve transection alters jaw-tongue coordination during mastication in pigs

Author:

Montuelle Stéphane J.1,Olson Rachel A.2,Curtis Hannah3,Williams Susan H.3ORCID

Affiliation:

1. Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, Warrensville Heights, Ohio

2. Department of Biological Sciences, Ohio University, Athens, Ohio

3. Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, Athens, Ohio

Abstract

During chewing, movements and deformations of the tongue are coordinated with jaw movements to manage and manipulate the bolus and avoid injury. Individuals with injuries to the lingual nerve report both tongue injuries due to biting and difficulties in chewing, primarily because of impaired bolus management, suggesting that jaw-tongue coordination relies on intact lingual afferents. Here, we investigate how unilateral lingual nerve (LN) transection affects jaw-tongue coordination in an animal model (pig, Sus scrofa). Temporal coordination between jaw pitch (opening-closing) and 1) anteroposterior tongue position (i.e., protraction-retraction), 2) anteroposterior tongue length, and 3) mediolateral tongue width was compared between pre- and post-LN transection using cross-correlation analyses. Overall, following LN transection, the lag between jaw pitch and the majority of tongue kinematics decreased significantly, demonstrating that sensory loss from the tongue alters jaw-tongue coordination. In addition, decrease in jaw-tongue lag suggests that, following LN transection, tongue movements and deformations occur earlier in the gape cycle than when the lingual sensory afferents are intact. If the velocity of tongue movements and deformations remains constant, earlier occurrence can reflect less pronounced movements, possibly to avoid injuries. The results of this study demonstrate that lingual afferents participate in chewing by assisting with coordinating the timing of jaw and tongue movements. The observed changes may affect bolus management performance and/or may represent protective strategies because of altered somatosensory awareness of the tongue. NEW & NOTEWORTHY Chewing requires coordination between tongue and jaw movements. We compared the coordination of tongue movements and deformation relative to jaw opening-closing movements pre- and post-lingual nerve transection during chewing in pigs. These experiments reveal that the timing of jaw-tongue coordination is altered following unilateral disruption of sensory information from the tongue. Therefore, maintenance of jaw-tongue coordination requires bilateral sensory information from the tongue.

Funder

HHS | NIH | National Institute of Dental and Craniofacial Research

NSF | BIO | Division of Integrative Organismal Systems

NSF | BIO | Division of Biological Infrastructure

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology

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