Neural substrates of de novo motor skill learning

Human motor skill learning is a complicated process of generating a novel movement pattern to achieve a task goal guided by evaluative feedback such as rewards. The Basal Ganglia (BG) plays a central role in reward-based motor skill learning. Recent primate studies suggest rostrocaudally separated circuits in the BG for voluntary (early) versus automatic (late) behavior. However, little has been known about the separate circuits of the BG in reward-based human motor skill learning.

To date, most neuroimaging studies investigating neural mechanism of motor skill learning have employed target-reaching, sequential force control, or sequence learning tasks. Here, we designed a novel fMRI experiment in which subjects learn a novel motor skill from scratch. Subjects wear a MR-compatible data-glove and learn to control a computer cursor over a 5-by-5 grid by manipulating fingers ( see figure).

We collected behavioral and fMRI data from more than 25 subjects. All individual learned to control a cursor to reach targets after extensive training (see figure below).

To investigate how extensive training changes neural representation of mapping between high-dimensional motor space and low-dimensional task space, subjects participated in two fMRI sessions separated by five training sessions. The extensive training decreased interaction between the motor and visual modules but increased interaction between the motor and reward modules. We also found the central executive, salience, and dorsal/ventral attention networks were strongly modulated by trial-by-trial reward in the early learning phase, but the extensive training reduced the sensitivity of these networks to the rewards.

Most interestingly, we found fMRI evidences supporting the separate circuits in the caudate nucleus for early versus late stage of motor skill learning. As a result of the extensive training, the reward-modulated region shifted from the rostral to the caudal part of the caudate nucleus. However, there was no such a change in cortical area, vmPFC.

To our best knowledge, for the first time, we report motor learning-induced transition of reward modulating regions of the human brain. In the future, we will use 7 T fMRI scanner to investigate the tail region of the caudate nucleus with higher spatial resolution. Additionally, we will use TMS targeting the primary motor cortex to understand how consolidation process would be modulated by the tail region of the caudate nucleus. (For downloading a poster presented in the annual meeting of Cognitive Neuroscience Society 2019, related this work, please click here)