Disengagement of Motor Cortex during Long-Term Learning Tracks the Performance Level of Learned Movements

Disengagement of Motor Cortex during Long-Term Learning Tracks the Performance Level of Learned Movements
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DOI:
10.1523/jneurosci.3049-20.2021
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发表时间:
2021-08-18
影响因子:
5.3
通讯作者:
Komiyama, Takaki
Komiyama, Takaki
中科院分区:
医学1区
文献类型:
--
作者:
Hwang, Eun Jung;Dahlen, Jeffrey E.;Komiyama, Takaki

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并不是所有的运动都需要运动皮层来完成。有趣的是,特定动作对运动皮层的依赖不是固定的,而是在长期学习过程中动态变化的。例如,啮齿动物的前肢运动最初需要运动皮层,经过长时间的训练后,可以独立于运动皮层。然而,目前尚不清楚长期的神经变化是否使运动皮层可缺性是训练时间的简单作用。为了解决这个问题,我们训练老鼠(雄性和雌性)在几个星期内同时进行两种不同的前肢运动,用操纵杆向前和向下伸展,然后比较运动皮层在这两种运动中的参与情况。经过长期训练,大多数小鼠在这两种运动之间达到了不同水平的运动表现。在这两种运动中,具有较高一致性的运动(即方向一致的运动)受运动皮层失活的影响明显小于另一种运动(即方向可变的运动)。运动皮质神经元的双光子钙成像显示,与可变方向运动相比,恒定方向运动激活的神经元较少,产生的群体活动更弱,一致性更差。总的来说,运动皮层对于达到更高水平一致性的习得运动的参与程度更低,也不那么必要。因此,将运动皮层从习得的运动中解放出来的神经回路的长期重组不仅仅是训练时间的作用。相反,这种重组会追踪动物在训练期间达到的运动表现水平。
Not all movements require the motor cortex for execution. Intriguingly, dependence on motor cortex of a given movement is not fixed, but instead can dynamically change over the course of long-term learning. For instance, rodent forelimb movements that initially require motor cortex can become independent of the motor cortex after an extended period of training. However, it remains unclear whether long-term neural changes rendering the motor cortex dispensable are a simple function of the training length. To address this issue, we trained mice (both male and female) to perform two distinct forelimb movements, forward versus downward reaches with a joystick, concomitantly over several weeks, and then compared the involvement of the motor cortex between the two movements. Most mice achieved different levels of motor performance between the two movements after long-term training. Of the two movements, the one that achieved higher trial-to-trial consistency (i.e., consistent-direction movement) was significantly less affected by inactivation of motor cortex than the other (i.e., variable-direction movement). Two-photon calcium imaging of motor cortical neurons revealed that the consistent-direction movement activates fewer neurons, producing weaker and less consistent population activity than the variable-direction movement. Together, the motor cortex was less engaged and less necessary for learned movements that achieved higher levels of consistency. Thus, the long-term reorganization of neural circuits that frees the motor cortex from the learned movement is not a mere function of training length. Rather, this reorganization tracks the level of motor performance that the animal achieves during training.