Differential activation of monkey striatal neurons in the early and late stages of procedural learning

Abstract

The basal ganglia is a key structure for procedural learning. To examine in what aspects of procedural learning the basal ganglia participate, we recorded from striatal neurons (phasically active neurons) in monkeys while the animals were performing a sequential button press task (the 2×5 task) and compared the neuronal activity between two conditions: (1) while learning new sequences and (2) while executing overlearned sequences. Among 147 neurons recorded in two monkeys, 45 neurons were activated preferentially for new sequences (new-preferring neurons), 34 for overlearned sequences (learned-preferring neurons), and 68 were activated non-selectively (non-selective neurons). New-preferring neurons were more abundant in the “association” region [association striatum (AS); caudate nucleus and rostral putamen anterior to the anterior commissure], while the learned-preferring neurons were more abundant in the “sensorimotor” region [sensorimotor striatum (SM); putamen posterior to the anterior commissure]. In addition to the learning dependency, the AS and SM neurons were activated in different task periods: many AS neurons were activated during the delay period, while the SM neurons were more activated with reaching and button presses. These data, together with the data from our previous blockade study, suggest that the “association” and “sensorimotor” regions of the basal ganglia contribute preferentially to the early and late stages of procedural learning, respectively.