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Features Of Cortically Evoked Swallowing In The Awake Primate (Macaca Fascicularis)

Ruth E. Martin, Pentti Kemppainen, Yuji Masuda, Dongyuan Yao, Gregory M. Murray, Barry J. Sessle

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Although the cerebral cortex has been implicated in the control of swallowing, the output organization of the cortical swallowing representation, and features of cortically evoked swallowing, remain unclear. The present study defined the output features of the primate “cortical swallowing representation” with intracortical microstimulation (ICMS) applied within the lateral sensorimotor cortex. In four hemispheres of two awake monkeys, microelectrode penetrations were made at ≤1-mm intervals, initially within the face primary motor cortex (face-MI), and subsequently within the cortical regions immediately rostral, lateral, and caudal to MI. Two ICMS pulse trains [35-ms train, 0.2-ms pulses at 333 Hz, ≤30 μA (short train stimulus, T/S); 3- to 4-s train, 0.2-ms pulses at 50 Hz, ≤60 μA (continuous stimulus, C/S)] were applied at ≤500-μm intervals along each microelectrode penetration to a depth of 8–10 mm, and electromyographic (EMG) activity was recorded simultaneously from various orofacial and laryngeal muscles. Evoked orofacial movements, including swallowing, were verified by EMG analysis, and T/S and C/S movement thresholds were determined. Effects of varying ICMS intensity on swallow-related EMG properties were examined by applying suprathreshold C/S at selected intracortical sites. EMG patterns of swallows evoked from various cortical regions were compared with those of natural swallows recorded as the monkeys swallowed liquid and solid material. Results indicated that swallowing was evoked by C/S at ∼20% of 1,569 intracortical sites where ICMS elicited an orofacial motor response in both hemispheres of the two monkeys, typically at C/S intensities ≤30 μA. In contrast, swallowing was not evoked by T/S in either monkey. Swallowing was evoked from four cortical regions: the ICMS-defined face-MI, the face primary somatosensory cortex (face-SI), the region lateral and anterior to face-MI corresponding to the cortical masticatory area (CMA), and an area >5 mm deep to the cortical surface corresponding to both the white matter underlying the CMA and the frontal operculum; EMG patterns of swallows elicited from these four cortical regions showed some statistically significant differences. Whereas swallowing only was evoked at some sites, particularly within the deep cortical area, swallowing was more frequently evoked together with other orofacial responses including rhythmic jaw movements. Increasing ICMS intensity increased the magnitude, and decreased the latency, of the swallow-related EMG burst in the genioglossus muscle at some sites. These findings suggest that a number of distinct cortical foci may participate in the initiation and modulation of the swallowing synergy as well as in integrating the swallow within the masticatory sequence.