Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity

Abstract

Primates can give behavioral responses on the basis of arbitrary, context-dependent rules. When sensory instructions and behavioral responses are associated by arbitrary rules, these rules need to be learned. This study investigates the temporal dynamics of functional segregation at the basis of visuomotor associative learning in humans, isolating specific learning-related changes in neurovascular activity across the whole brain. We have used fMRI to measure human brain activity during performance of two tasks requiring the association of visual patterns with motor responses. Both tasks were learned by trial and error, either before (visuomotor control) or during (visuomotor learning) the scanning session. Epochs of tasks performance (∼30 s) were alternated with a baseline period over the whole scanning session (∼50 min). We have assessed both linear and nonlinear modulations in the differential signal between tasks, independently from overall task differences. The performance indices of the visuomotor learning task smoothly converged onto the values of a steady-state control condition, according to nonlinear timecourses. Specific visuomotor learning-related activity has been found over a distributed cortical network, centred on a temporo-prefrontal circuit. These cortical time-modulated activities were supported early in learning by the hippocampal/parahippocampal complex, and late in learning by the basal ganglia system. These findings suggest the inferior temporal and the ventral prefrontal cortex are critical neural nodes for integrating perceptual information with executive processes.