The Journal of Neurophysiology Vol. 78 No. 3 September 1997, pp. 1516-1530
Copyright ©1997 The American Physiological Society

Functional Properties of Neurons in the Primate Tongue Primary Motor Cortex During Swallowing

Ruth E. Martin¹, Gregory M. Murray², Pentti Kemppainen³, Yuji Masuda⁴, and Barry J. Sessle⁵

¹ Faculty of Applied Health Sciences, University of Western Ontario, London, Ontario N6G 1H1; ² Faculty of Dentistry, University of Sydney, Sydney, New South Wales, Australia 2010; ³ Department of Prosthetic Dentistry, University of Helsinki, 00014 Helsinki, Finland; ⁴ Faculty of Dentistry, Osaka University, Osaka 565, Japan; and ⁵ Faculty of Dentistry, University of Toronto, Toronto, Ontario M5G 1G6, Canada

Martin, Ruth E., Gregory M. Murray, Pentti Kemppainen, Yuji Masuda, and Barry J. Sessle. Functional properties of neurons in the primate tongue primary motor cortex during swallowing.J. Neurophysiol. 78: 1516-1530, 1997. Recent studies conducted in our laboratory have suggested that the tongue primary motor cortex (i.e., tongue-MI) plays a critical role in the control of voluntary tongue movements in the primate. However, the possible involvement of tongue-MI in semiautomatic tongue movements, such as those in swallowing, remains unkown. Therefore the present study was undertakein in attempts to address whether tongue-MI plays a role in the semiautomatic tongue movements produced during swallowing. Extracellular single neuron recordings were obtained from tongue-MI, defined by intracortical microstimulation (ICMS), in two awake monkeys as they performed three types of swallowing (swallowing of a juice reward after successful tongue task performance, nontask-related swallowing of a liquid bolus, and nontask-related swallowing of a solid bolus) as well as a trained tongue-protrusion task. Electromyographic activity was recorded simultaneously from various orofacial and laryngeal muscles. In addition, the afferent input to each tongue-MI neuron and ICMS-evoked motor output characteristics at each neuronal recording site were determined. Neurons were considered to show swallow and/or tongue-protrusion task-related activity if a statistically significant difference in firing rate was seen in association with these behaviors compared with that observed during a control pretrial period. Of a total of 80 neurons recorded along 40 microelectrode penetrations in the ICMS-defined tongue-MI, 69% showed significant alterations of activity in relation to the swallowing of a juice reward, whereas 66% exhibited significant modulations of firing in association with performance of the trained tongue-protrusion task. Moreover, 48% showed significant alterations of firing in relation to both swallowing and the tongue-protrusion task. These findings suggest that the region of cortex involved in swallowing includes MI and that tongue-MI may play a role in the regulation of semiautomatic tongue movement, in addition to trained motor behavior. Swallow-related tongue-MI neurons exhibited a variety of swallow-related activity patterns and were distributed throughout the ICMS-defined tongue-MI at sites where ICMS evoked a variety of types of tongue movements. These findings are consistent with the view that multiple efferent zones for the production of tongue movements are activated in swallowing. Many swallow-related tongue-MI neurons had an orofacial mechanoreceptive field, particularly on the tongue dorsum, supporting the view that afferent inputs may be involved in the regulation of the swallowing synergy.

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