Stimulus selection drives value-modulated somatosensory processing in superior colliculus

Abstract

A fundamental trait of intelligent behavior is the ability to respond selectively to stimuli with higher value. Where along the somatosensory hierarchy does information transition from a map of stimulus location to a map of stimulus value? To address this question, we recorded single-unit activity from populations of neurons in somatosensory cortex (S1) and midbrain superior colliculus (SC) in mice conditioned to respond to a positive-valued whisker stimulus and withhold responses using an adjacent, negative-valued whisker stimulus. The stimulus preference of the S1 population was equally weighted towards either whisker, in line with a somatotopic map. Surprisingly, we discovered a large population of SC neurons that were disproportionately biased towards the positive stimulus. This disproportionate bias was controlled by spike facilitation for the positive stimulus and spike suppression for the negative stimulus in single neurons. Removing the opportunity for mice to select the positive stimulus reduced stimulus bias in SC but not S1, suggesting that sensory processing in SC neurons was partially controlled by movement preparation. Similarly, the spontaneous firing rates of SC but not S1 neurons accurately predicted reaction times, suggesting that SC neurons play a persistent role in perceptual decision-making. Taken together, these data indicate that the somatotopic map in S1 is transformed into a value-based map in SC that encodes stimulus priority.