Encoding of Reward and Decoding Movement from the Frontal Eye Field during Smooth Pursuit Eye Movements

Expectation of reward potentiates sensorimotor transformations to drive vigorous movements. One of the main challenges in studying reward is to determine how representations of reward interact with the computations that drive behavior. We recorded activity in smooth pursuit neurons in the frontal eye field (FEF) of two male rhesus monkeys while controlling the eye speed by manipulating either reward size or target speed. The neurons encoded the different reward conditions more strongly than the different target speed conditions. This pattern could not be explained by differences in the eye speed, since the eye speed sensitivity of the neurons was also larger for the reward conditions. Pooling the responses by the preferred direction of the neurons attenuated the reward modulation and led to a tighter association between neural activity and behavior. Therefore, a plausible decoder such as the population vector could explain how the FEF both drives behavior and encodes reward beyond behavior. SIGNIFICANCE STATEMENT Motor areas combine sensory and reward information to drive movement. To disambiguate these sources, we manipulated the speed of smooth pursuit eye movements by controlling either the size of the reward or the speed of the visual motion signals. We found that the relationship between activity in frontal eye field and eye kinematics varied: the eye speed sensitivity was larger for the different reward conditions than for the different target speed conditions. Decoders that pooled signals by the preferred direction of the neurons attenuated the reward modulations. These decoders may indicate how reward can be both encoded beyond eye kinematics at the single neuron level and drive movement at the population level.