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吞咽过程中灵长类动物舌部初级运动皮层神经元的功能特性

Functional properties of neurons in the primate tongue primary motor cortex during swallowing.

作者信息

Martin R E, Murray G M, Kemppainen P, Masuda Y, Sessle B J

机构信息

Faculty of Applied Health Sciences, University of Western Ontario, London, Canada.

出版信息

J Neurophysiol. 1997 Sep;78(3):1516-30. doi: 10.1152/jn.1997.78.3.1516.

DOI:10.1152/jn.1997.78.3.1516
PMID:9310440
Abstract

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 unknown. Therefore the present study was undertaken 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.

摘要

我们实验室最近进行的研究表明,舌部初级运动皮层(即舌部-运动皮层)在灵长类动物自主舌部运动的控制中起着关键作用。然而,舌部-运动皮层是否参与半自动舌部运动,如吞咽时的运动,仍不清楚。因此,本研究旨在探讨舌部-运动皮层在吞咽过程中产生的半自动舌部运动中是否发挥作用。在两只清醒的猴子执行三种吞咽任务(成功完成舌部任务后吞咽果汁奖励、与任务无关的液体团块吞咽以及与任务无关的固体团块吞咽)以及一项训练有素的伸舌任务时,通过皮层内微刺激(ICMS)定义舌部-运动皮层,并从该区域获得细胞外单神经元记录。同时记录各种口面部和喉部肌肉的肌电图活动。此外,还确定了每个舌部-运动皮层神经元的传入输入以及每个神经元记录部位的ICMS诱发运动输出特征。如果与对照预试验期相比,在这些行为相关的放电率上观察到统计学上的显著差异,则认为神经元表现出与吞咽和/或伸舌任务相关的活动。在ICMS定义的舌部-运动皮层中,沿着40个微电极穿刺记录的总共80个神经元中,69%的神经元在吞咽果汁奖励时表现出显著的活动变化,而66%的神经元在执行训练有素的伸舌任务时表现出显著的放电调制。此外,48%的神经元在吞咽和伸舌任务中均表现出显著的放电变化。这些发现表明,参与吞咽的皮层区域包括运动皮层,并且舌部-运动皮层除了在训练有素的运动行为中发挥作用外,可能还在半自动舌部运动的调节中发挥作用。与吞咽相关的舌部-运动皮层神经元表现出多种与吞咽相关的活动模式,并且分布在ICMS定义的舌部-运动皮层中,在这些部位ICMS诱发了多种类型的舌部运动。这些发现与以下观点一致,即吞咽时会激活多个产生舌部运动的传出区域。许多与吞咽相关的舌部-运动皮层神经元具有口面部机械感受野,特别是在舌背,这支持了传入输入可能参与吞咽协同作用调节的观点。

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