Encoding of motor sequences in primate globus pallidus and motor cortex: Uniform preference for ordinal position

Abstract

How the brain organizes discrete actions into fluid sequences is a central problem in motor neuroscience. Competing models of basal ganglia (BG) function propose that BG neurons either signal sequence boundaries or encode movements across ordinal positions. Prior studies have largely examined fixed sequences with end-of-sequence rewards, leaving open whether such findings generalize to more naturalistic conditions. We trained four rhesus macaques to perform a visuomotor sequence task requiring four or five out-and-back joystick movements to peripheral targets. Sequences were completed under two conditions: a random condition, in which target order varied across trials, and a fixed condition, in which order was predictable and consistent. Rewards were delivered after each movement, dissociating reward timing from sequence completion. We recorded single-unit activity in arm-related regions of the globus pallidus (GP; n = 458) and primary motor cortex (M1; n = 306). Regression analyses revealed that many neurons in both GP and M1 encoded ordinal position within a sequence. Order effects were more frequent in the fixed condition, but were also present during random sequences. We found no evidence for preferential encoding of sequence initiation or termination in overlearned sequences, in contrast to prior studies reporting start/stop signals in basal ganglia. Weak effects appeared under the random condition in one animal pair, but these did not generalize across animals or conditions. Instead, neurons exhibited heterogeneous order-related responses spanning the full sequence. These results demonstrate that GP neurons, like those in M1, encode ordinal position throughout a sequence rather than acting solely as sequence initiators or terminators. This challenges boundary-specific models of BG function and highlights the BGs broader role in representing serial order during motor sequence production.