Signaling the agency of an erroneous outcome via synchronization of spikes in the cerebellum

Abstract

Neurons in the inferior olive are thought to anatomically organize the Purkinje cells (P-cells) of the cerebellum into computational modules. To better understand what is computed by these modules, we designed a saccade task in marmosets that dissociated sensory and motor events and then recorded the complex and simple spikes of hundreds of P-cells. We found that when a visual target was presented at a random location, the olive reported the direction of that sensory event to one group of P-cells, but not to a second group. However, just before movement onset it reported the direction of the planned movement to both groups, even if that movement was not toward the target. At the end of the movement if there was an error but the subject chose to withhold the corrective movement, only the first group received information about the sensory prediction error. We organized the P-cells based on the information content of their olivary input and found that in the group that received sensory information, the simple spikes were suppressed during fixation, then produced a burst before saccade onset in a direction consistent with assisting the movement. In the second group the simple spikes were not suppressed during fixation but burst near saccade deceleration in a direction consistent with stopping the movement. Thus, the olive differentiated the P-cells based on whether they would receive sensory or motor information, and this defined their contributions to control of movements as well as holding still. Significance statementWe found that in the oculomotor region of the vermis, the olive informed a subset of P-cells about sensory events that were prediction errors, but all P-cells about the forthcoming movement. Using the information content of the olivary input we labeled the P-cells and produced a population code, revealing two groups with simple spikes that were antagonistic to each other, one contributing to movement initiation, the other signaling movement end.