Frontal and Parietal Contributions to Proprioception and Motor Skill Learning

Abstract

Motor skill learning is the process of developing new movements with practice until they can be performed automatically. This necessitates the interaction of high-level cognitive processes with low-level sensorimotor mechanisms. Skill learning involves not only changes in the motor system but also proprioception (position sense). Proprioceptive deficits increase variability and decrease accuracy of movement. The somatosensory cortex, where low-level proprioception is processed, is known to play a role in motor skill learning, but the involvement of higher-level proprioceptive regions is unclear. Dorsolateral prefrontal cortex (DLPFC) has been linked to the high-level early stages of motor learning, and indirectly to proprioception. Supramarginal gyrus (SMG), an interface area between motor and sensory cortices, has been linked to higher-order proprioceptive processing. In this study, we asked how activity in DLPFC and SMG influences motor skill learning. Participants learned an upper limb motor skill designed to be spatially complex and dependent on proprioception: tracing a two-dimensional maze as accurately as possible within the desired speed range, using a KINARM Endpoint robotic manipulandum. Proprioceptive acuity (sensitivity and bias) was assessed before and after continuous theta burst transcranial magnetic stimulation (cTBS) was applied to inhibit activity in DLPFC, SMG, or Sham. To measure motor skill, movement accuracy and variability were examined at the trained speed as well as at a faster (more difficult) and a slower (easier) speed. Skill was assessed before and after cTBS, after 40 training trials (early learning) and after another 80 trials (late learning). All three groups showed improvements in movement accuracy and variance, indicating they learned the maze tracing skill. However, the Sham group improved movement variability at the faster speed significantly more than the DLPFC or SMG groups did. This suggests that DLPFC and SMG are important for the more challenging aspects of motor skill learning, consistent with their association with higher-level proprioceptive function.