Cortical neural modulation by previous trial outcome differentiates fast-from slow-learning rats on a visuomotor directional choice task

Abstract

To better understand the neural cortical underpinnings that explain behavioral differences in learning rate, we recorded single-unit activity in primary motor (M1) and secondary motor (M2) areas while rats learned to perform a directional (left or right) operant visuomotor association task. Analysis of neural activity during the early portion of the cue period showed that neural modulation in the motor cortex was most strongly associated with two task factors: the previous trial outcome (success or error) and the current trial’s directional choice (left or right). Furthermore, the fast learners, defined as those who had steeper learning curves and required fewer learning sessions to reach criterion performance, encoded the previous trial outcome factor more strongly than the directional choice factor. Conversely, the slow learners encoded directional choice more strongly than previous trial outcome. These differences in task factor encoding were observed in both the percentage of neurons and the neural modulation depth. These results suggest that fast learning is accompanied by a stronger component of previous trial outcome in the modulation representation present in motor cortex, which therefore may be a contributing factor to behavioral differences in learning rate. NEW & NOTEWORTHY We chronically recorded neural activity as rats learned a visuomotor directional choice task from a naive state. Learning rates varied. Single-unit neural modulation of two motor areas revealed that the fast learners encoded previous trial outcome more strongly than directional choice, whereas the reverse was true for slow learners. This finding provides novel evidence that rat learning rate is strongly correlated with the strength of neural modulation by previous trial outcome in motor cortex.