Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling.
We dissociated the contributions to learning of four corticostriatal "loops" (interacting striatal and cortical regions): motor (putamen and motor cortex), visual (posterior caudate and visual cortex), executive (anterior caudate and prefrontal cortex), and motivational (ventral striatum and ventromedial frontal cortex). Subjects learned to categorize individual repeated images into one of two arbitrary categories via trial and error. We identified (1) regions sensitive to correct categorization, categorization learning, and feedback valence; (2) regions sensitive to prediction error (violation of feedback expectancy) and reward prediction (expected feedback associated with category response) using reinforcement learning modeling; and (3) directed influences between regions using Granger causality modeling. Each loop showed a unique pattern of sensitivity to each of these factors. Both the motor and visual loops were involved in acquisition of categorization ability: activity during correct categorization increased across learning and was sensitive to reward prediction. However, the posterior caudate received directed influence from visual cortex, whereas the putamen exerted directed influence on motor cortex. The motivational and executive loops were involved in feedback processing: both regions were sensitive to feedback valence, which interacted with learning across scans. However, the motivational loop activity reflected prediction error, whereas executive loop activity reflected reward prediction, consistent with the executive loop role in integrating reward and action. Granger causality modeling found directed influences between striatal and cortical regions within each loop. Across loops, the motor loop exerted directed influence on the executive loop which is consistent with the role of the executive loop in integrating feedback with stimulus-response history.
Seger
Carol A
CA
Department of Psychology, Colorado State University, Fort Collins, CO 80523, USA. Carol.Seger@colostate.edu
Peterson
Erik J
EJ
Cincotta
Corinna M
CM
Lopez-Paniagua
Dan
D
Anderson
Charles W
CW
D001921:Brain / Q000502:physiology*; D001931:Brain Mapping; D005260:Female; D006801:Humans; D007090:Image Interpretation, Computer-Assisted; D007858:Learning / Q000502:physiology*; D008279:Magnetic Resonance Imaging; D008297:Male; D008959:Models, Neurological; D008962:Models, Theoretical