Cerebellar roles in frequency competitive motor learning of the vestibulo-ocular reflex

Cerebellar roles in frequency competitive motor learning of the vestibulo-ocular reflex
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小脑在前庭眼反射频率竞争性运动学习中的作用

DOI:
10.1016/j.neuroscience.2020.09.016
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发表时间:
2021
期刊:
Neurosicence
影响因子:
--
通讯作者:
Y.
Y.
中科院分区:
--
文献类型:
--
作者:
Soga;J.;Matsuyama;M.;Miura;H.;Highstein;S.;Baker;R.;Hirata;Y.

文献摘要

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生物运动通常包含多个频率成分,其中每个基本成分都必须通过运动学习来调整,以获得新的运动技能或保持已获得的技能。在此电机性能期间,有时需要增强一个频率分量(增益上升),而另一个频率分量则被抑制(增益下降)。这种同时在不同频率上下调整的模式被称为频率竞争性运动学习。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。先前,灵长类动物的VOR运动学习表现为频率选择性和频率竞争性运动学习。在这里,我们证明金鱼VOR进行频率竞争运动学习时,高和低的频率成分分别训练为增益和增益下降。然而,当两个频率分量在相反的方向上训练时,只观察到增益分量。我们还发现,小脑切除术排除了任何频率竞争性VOR运动学习。来自前庭-小脑浦肯野细胞的补充单单元记录显示,随着增益-下降学习,放电调制发生了变化,而增益-上升学习与频率无关。这些结果表明,所有频率竞争性VOR运动学习都需要小脑,其中的浦肯野细胞活性与所有独立于频率的增益-下降行为密切相关。然而,频率竞争增益学习需要完整的、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上升和下降学习利用单独的脑干/小脑回路,反过来,这显然是动眼肌系统处理多频率成分的独特能力的基础。
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.