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Translating rewards to eye movements

Periodic Reporting for period 3 - iMove (Translating rewards to eye movements)

Período documentado: 2021-07-01 hasta 2022-12-31

The brain uses two major subcortical networks to drive behavior: the basal ganglia and the cerebellum. Both areas are essential for the control of movement as damage to either structure leads to severe motor disabilities. Research on the basal ganglia has highlighted their importance in the control of reward-driven behavior, but the ways in which the reward information interacts with sensorimotor signals to drive the motor periphery is unknown. By contrast, research on the cerebellum has focused primarily on how sensory error signals are used to optimize motor commands but has mostly ignored the modulatory factors that influence behavior, such as reward. My goal is to unify research on the basal ganglia and cerebellum to understand how the computations underlying the influence of reward on action are implemented in the brain.
Our initial research focused on studying reward and eye movements in the cerebellum. We have completed the data collection for this aim and have published three papers based on these results. We are now expanding our initial findings in the cerebellum and studying the basal ganglia.
Summary of the main results:
Activity of the Climbing fibers in the cerebellum. Climbing fiber inputs to the cerebellum encode error signals that instruct learning. We examined whether rewarding events are encoded in these spikes. We recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial the monkeys were cued the size of reward that would be delivered upon successful completion of the trial. We found increased climbing fiber activity during cue presentation when information about reward size was first made available. Reward size did not modulate activity at reward delivery. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction. These results were published in eLife.

Activity of simple spikes in the cerebellum. To test how reward-related signals interact with sensorimotor processing in the cerebellum we recorded Purkinje cell simple spike activity in the cerebellar floccular complex while monkeys were engaged in smooth pursuit eye movement tasks. Here we focused solely on the activity of neurons that encode the parameters of eye movement. Consistent with previous research we identified reward-related simple spike modulations during movement. Notably, the size of the reward-related modulation matched the size of the effect of reward on behavior. We exploited the well-established relationship between eye movement parameters and neural activity in the cerebellum to show that coding of the eye kinematics explains these reward-related modulations. The modulation in activity did not seem to arise from the complex spike reward modulations since they were distinct in time and there were fewer in the neurons that encoded eye movements. These results suggest that the transformation of reward information to movement is already completed at the level of the Purkinje cells in the floccular complex. A paper that summarizes these results was published in the Journal of Neurophysiology.
In the second half of the project, we will focus on the completion of aim 2 and the execution of aim 3. We have already started pursuing aim 3 at the technical level in which we plan to perform optogenetic experiments in monkeys to study pathways from the frontal cortex to the basal ganglia.