Reward Modulates Visual Responses in the Superficial Superior Colliculus of Mice

Abstract

The processing of sensory input is constantly adapting to behavioral demands and internal states. The drive to obtain reward, e.g., searching for water when thirsty, is a strong behavioral demand and associating the reward with its source, a certain environment or action, is paramount for survival. Here, we show that water reward increases subsequent visual activity in the superficial layers of the superior colliculus (SC), which receive direct input from the retina and belong to the earliest stages of visual processing. We trained mice of either sex to perform a visual decision task and recorded the activity of neurons in the SC using two-photon calcium imaging and high-density electrophysiological recordings. Responses to visual stimuli in around 20% of visually responsive neurons in the superficial SC were affected by reward delivered in the previous trial. Reward mostly increased visual responses independent from modulations due to pupil size changes. The modulation of visual responses by reward could not be explained by movements like licking. It was specific to responses to the following visual stimulus, independent of slow fluctuations in neural activity and independent of how often the stimulus was previously rewarded. Electrophysiological recordings confirmed these results and revealed that reward affected the early phase of the visual response around 80 ms after stimulus onset. Modulation of visual responses by reward, but not pupil size, significantly improved the performance of a population decoder to detect visual stimuli, indicating the relevance of reward modulation for the visual performance of the animal.SIGNIFICANCE STATEMENTTo learn which actions lead to food, water, or safety, it is necessary to integrate the receiving of reward with sensory stimuli related to the reward. Cortical stages of sensory processing have been shown to represent stimulus-reward associations. Here, we show, however, that reward influences neurons at a much earlier stage of sensory processing, the superior colliculus (SC), receiving direct input from the retina. Visual responses were increased shortly after the animal received the water reward, which led to an improved stimulus signal in the population of these visual neurons. Reward modulation of early visual responses may thus improve perception of visual environments predictive of reward.