Sidarta Ananda, Vahdat Shahabeddin, Bernardi Nicolò F, Ostry David J
Department of Psychology, McGill University, Montreal, Quebec H3A 1B1, Canada.
Functional Neuroimaging Unit, University of Montreal, Montreal, Quebec H3T 1J4, Canada, and.
J Neurosci. 2016 Nov 16;36(46):11682-11692. doi: 10.1523/JNEUROSCI.1767-16.2016.
As one learns to dance or play tennis, the desired somatosensory state is typically unknown. Trial and error is important as motor behavior is shaped by successful and unsuccessful movements. As an experimental model, we designed a task in which human participants make reaching movements to a hidden target and receive positive reinforcement when successful. We identified somatic and reinforcement-based sources of plasticity on the basis of changes in functional connectivity using resting-state fMRI before and after learning. The neuroimaging data revealed reinforcement-related changes in both motor and somatosensory brain areas in which a strengthening of connectivity was related to the amount of positive reinforcement during learning. Areas of prefrontal cortex were similarly altered in relation to reinforcement, with connectivity between sensorimotor areas of putamen and the reward-related ventromedial prefrontal cortex strengthened in relation to the amount of successful feedback received. In other analyses, we assessed connectivity related to changes in movement direction between trials, a type of variability that presumably reflects exploratory strategies during learning. We found that connectivity in a network linking motor and somatosensory cortices increased with trial-to-trial changes in direction. Connectivity varied as well with the change in movement direction following incorrect movements. Here the changes were observed in a somatic memory and decision making network involving ventrolateral prefrontal cortex and second somatosensory cortex. Our results point to the idea that the initial stages of motor learning are not wholly motor but rather involve plasticity in somatic and prefrontal networks related both to reward and exploration.
In the initial stages of motor learning, the placement of the limbs is learned primarily through trial and error. In an experimental analog, participants make reaching movements to a hidden target and receive positive feedback when successful. We identified sources of plasticity based on changes in functional connectivity using resting-state fMRI. The main finding is that there is a strengthening of connectivity between reward-related prefrontal areas and sensorimotor areas in the basal ganglia and frontal cortex. There is also a strengthening of connectivity related to movement exploration in sensorimotor circuits involved in somatic memory and decision making. The results indicate that initial stages of motor learning depend on plasticity in somatic and prefrontal networks related to reward and exploration.
当一个人学习跳舞或打网球时，期望达到的体感状态通常是未知的。由于运动行为是由成功和不成功的动作塑造的，试错很重要。作为一个实验模型，我们设计了一项任务，让人类参与者向一个隐藏目标做出伸手动作，并在成功时获得正强化。我们根据学习前后静息态功能磁共振成像（fMRI）功能连接的变化，确定了基于躯体和强化的可塑性来源。神经影像学数据显示，运动和体感脑区都出现了与强化相关的变化，其中连接性的增强与学习过程中的正强化量有关。前额叶皮层区域也因强化而发生了类似的改变，壳核感觉运动区域与奖励相关的腹内侧前额叶皮层之间的连接性随着收到的成功反馈量而增强。在其他分析中，我们评估了与试验间运动方向变化相关的连接性，这种变化类型可能反映了学习过程中的探索策略。我们发现，连接运动和体感皮层的网络中的连接性随着方向的逐次试验变化而增加。连接性也随错误动作后的运动方向变化而变化。在这里，变化出现在一个涉及腹外侧前额叶皮层和第二体感皮层的躯体记忆和决策网络中。我们的结果表明，运动学习的初始阶段并非完全是运动性的，而是涉及与奖励和探索相关的躯体和前额叶网络的可塑性。
在运动学习的初始阶段，肢体的位置主要通过试错来学习。在一个实验模拟中，参与者向一个隐藏目标做出伸手动作，并在成功时获得正反馈。我们使用静息态fMRI根据功能连接的变化确定了可塑性来源。主要发现是，奖励相关的前额叶区域与基底神经节和额叶皮层的感觉运动区域之间的连接性增强。在涉及躯体记忆和决策的感觉运动回路中，与运动探索相关的连接性也增强。结果表明，运动学习的初始阶段依赖于与奖励和探索相关的躯体和前额叶网络的可塑性。
