Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois 60637, Committees on Computational Neuroscience and Neurobiology, University of Chicago, Chicago, Illinois 60637, and Faculty of Dentistry, University of Toronto, Toronto, Ontario M5G 1G6, Canada.
J Neurosci. 2014 Apr 23;34(17):5985-97. doi: 10.1523/JNEUROSCI.4367-13.2014.
The orofacial sensorimotor cortex is known to play a role in motor learning. However, how motor learning changes the dynamics of neuronal activity and whether these changes differ between orofacial primary motor (MIo) and somatosensory (SIo) cortices remain unknown. To address these questions, we used chronically implanted microelectrode arrays to track learning-induced changes in the activity of simultaneously recorded neurons in MIo and SIo as two naive monkeys (Macaca mulatta) were trained in a novel tongue-protrusion task. Over a period of 8-12 d, the monkeys showed behavioral improvements in task performance that were accompanied by rapid and long-lasting changes in neuronal responses in MIo and SIo occurring in parallel: (1) increases in the proportion of task-modulated neurons, (2) increases in the mutual information between tongue-protrusive force and spiking activity, (3) reductions in the across-trial firing rate variability, and (4) transient increases in coherent firing of neuronal pairs. More importantly, the time-resolved mutual information in MIo and SIo exhibited temporal alignment. While showing parallel changes, MIo neurons exhibited a bimodal distribution of peak correlation lag times between spiking activity and force, whereas SIo neurons showed a unimodal distribution. Moreover, coherent activity between pairs of MIo neurons was higher and centered around force onset compared with pairwise coherence of SIo neurons. Overall, the results suggest that the neuroplasticity in MIo and SIo occurring in parallel serves as a substrate for linking sensation and movement during sensorimotor learning, whereas the differing dynamic organizations reflect specific ways to control movement parameters as learning progresses.
口面感觉运动皮层已知在运动学习中起作用。然而，运动学习如何改变神经元活动的动力学，以及这些变化是否在口面运动初级皮层（MIo）和体感皮层（SIo）之间有所不同，目前尚不清楚。为了解决这些问题，我们使用慢性植入的微电极阵列来跟踪两只未经训练的猴子（猕猴）在一项新的舌伸出任务中学习过程中同时记录的 MIo 和 SIo 中神经元活动的变化。在 8-12 天的时间里，猴子在任务表现上表现出行为上的改善，同时 MIo 和 SIo 中的神经元反应也出现了快速而持久的变化：（1）任务调节神经元的比例增加；（2）舌伸出力和放电活动之间的互信息增加；（3）跨试验发放率变异性降低；（4）神经元对的相干发放增加。更重要的是，MIo 和 SIo 中的时变互信息表现出时间上的对齐。虽然表现出并行变化，但 MIo 神经元的放电活动和力之间的峰值相关滞后时间呈双峰分布，而 SIo 神经元呈单峰分布。此外，MIo 神经元对之间的相干活动比 SIo 神经元对之间的相干活动更高，并且集中在力的起始时。总体而言，结果表明，MIo 和 SIo 中同时发生的神经可塑性是将感觉和运动联系起来的基础在感觉运动学习过程中，而不同的动态组织反映了随着学习的进展控制运动参数的特定方式。
