Department of Computer Science, Chubu University Graduate School of Engineering, Japan.
Marine Biological Laboratory, United States.
Neuroscience. 2021 May 10;462:205-219. doi: 10.1016/j.neuroscience.2020.09.016. Epub 2020 Sep 15.
Biological motions commonly contain multiple frequency components in which each fundamental has to be adjusted by motor learning to acquire a new motor skill or maintain acquired skills. At times during this motor performance one frequency component needs to be enhanced (gain-up) while another is suppressed (gain-down). This pattern of simultaneous gain-up and -down adjustments at different frequencies is called frequency competitive motor learning. Currently we investigated cerebellar roles in this behavior utilizing the goldfish vestibulo-ocular reflex (VOR). Previously, VOR motor learning was shown in primates to be frequency selective and exhibit frequency competitive motor learning. Here we demonstrate that the goldfish VOR performs frequency competitive motor learning when high and low frequency components are trained to gain-up and gain-down, respectively. However, when the two frequency components were trained in the opposite directions only gain-up component was observed. We also found that cerebellectomy precluded any frequency competitive VOR motor learning. Complementary single unit recordings from vestibulo-cerebellar Purkinje cells revealed changes in firing modulation along with gain-down learning, but not with gain-up learning irrespective of frequency. These results demonstrate that the cerebellum is required for all frequency competitive VOR motor learning and Purkinje cell activity therein is well correlated with all gain-down behaviors independent of frequency. However, frequency competitive gain-up learning requires intact, recursive brainstem/cerebellar pathways. Collectively these findings support the idea that VOR gain-up and gain-down learning utilize separate brainstem/cerebellar circuitry that, in turn, clearly underlies the unique ability of the oculomotor system to deal with multiple frequency components.
生物运动通常包含多个频率分量，其中每个基本分量都必须通过运动学习进行调整，以获得新的运动技能或维持已获得的技能。在这种运动表现过程中，有时需要增强（增益上升）一个频率分量，同时抑制（增益下降）另一个频率分量。这种在不同频率下同时进行增益上升和下降调整的模式称为频率竞争运动学习。目前，我们利用金鱼前庭眼反射（VOR）研究了小脑在这种行为中的作用。以前，在灵长类动物中已经表明 VOR 运动学习是频率选择性的，并表现出频率竞争运动学习。在这里，我们证明当高、低频率分量分别进行增益上升和增益下降训练时，金鱼 VOR 会进行频率竞争运动学习。然而，当两个频率分量以相反的方向进行训练时，只观察到增益上升分量。我们还发现，小脑切除术排除了任何频率竞争 VOR 运动学习。来自前庭小脑浦肯野细胞的补充单细胞记录显示，在进行增益下降学习时，放电调制发生变化，但在进行增益上升学习时则没有变化，而无论频率如何。这些结果表明，小脑是所有频率竞争 VOR 运动学习所必需的，其中浦肯野细胞的活动与所有频率无关的增益下降行为密切相关。然而，频率竞争的增益上升学习需要完整的、递归的脑干/小脑通路。总的来说，这些发现支持了这样一种观点，即 VOR 的增益上升和增益下降学习利用了单独的脑干/小脑回路，而这反过来又明确地构成了眼球运动系统处理多个频率分量的独特能力的基础。
