Learning reduces variability but variability can facilitate learning. This paradoxical relationship has made it challenging to tease apart sources of variability that degrade performance from those that improve it. We tackled this question in a context-dependent timing task requiring humans and monkeys to flexibly produce different time intervals with different effectors. Subjects’ timing variability featured two novel and context-specific sources of variability: (1) slow memory-contingent fluctuations of the mean that degraded performance, and (2) fast reinforcement-dependent regulation of variance that improved performance. Signatures of these processes were evident across populations of neurons in multiple nodes of the cortico-basal ganglia circuits. However, only in a region of the thalamus involved in flexible control of timing were the slow performance-degrading fluctuations aligned to performance-optimizing regulation of variance. These findings provide direct evidence that the nervous system makes strategic use of exploratory variance to guard against other undesirable sources of variability.
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