Complementary Roles of Primate Dorsal Premotor and Pre-Supplementary Motor Areas to the Control of Motor Sequences

Abstract

We are able to temporally organize multiple movements in a purposeful manner in everyday life. Both the dorsal premotor (PMd) area and pre-supplementary motor area (pre-SMA) are known to be involved in the performance of motor sequences. However, it is unclear how each area differentially contributes to controlling multiple motor sequences. To address this issue, we recorded single-unit activity in both areas while monkeys (one male, one female) performed sixteen motor sequences. Each sequence comprised either a series of two identical movements (repetition) or two different movements (nonrepetition). The sequence was initially instructed with visual signals but had to be remembered thereafter. Here, we showed that the activity of single neurons in both areas transitioned from reactive- to predictive encoding while motor sequences were memorized. In the memory-guided trials, in particular, the activity of PMd cells preferentially represented the second movement (2M) in the sequence leading to a reward generally regardless of the first movement (1M). Such activity frequently began even before the 1M in a prospective manner, and was enhanced in nonrepetition sequences. Behaviorally, a lack of the activity enhancement often resulted in premature execution of the 2M. In contrast, cells in pre-SMA instantiated particular sequences of actions by coordinating switching or nonswitching movements in sequence. Our findings suggest that PMd and pre-SMA play complementary roles within behavioral contexts: PMd preferentially controls the movement that leads to a reward rather than the sequence per se, whereas pre-SMA coordinates all elements in a sequence by integrating temporal orders of multiple movements.

SIGNIFICANCE STATEMENT Although both dorsal premotor (PMd) area and pre-supplementary motor area (pre-SMA) are involved in the control of motor sequences, it is not clear how these two areas contribute to coordination of sequential movements differently. To address this issue, we directly compared neuronal activity in the two areas recorded while monkeys memorized and performed multiple motor sequences. Our findings suggest that PMd preferentially controls the final action that ultimately leads to a reward in a prospective manner, whereas the pre-SMA coordinates switching among multiple actions within the context of the sequence. Our findings are of significance to understand the distinct roles for motor-related areas in the planning and executing motor sequences and the pathophysiology of apraxia and/or Parkinson's diseases that disables skilled motor actions.