Spatial representations in the superior colliculus are modulated by competition among targets

Selecting and moving to spatial targets are critical components of goal-directed behavior, yet their neural bases are not well understood. The superior colliculus (SC) is thought to contain a topographic map of contralateral space in which the activity of specific neuronal populations corresponds to particular spatial locations. However, these spatial representations are modulated by several decision-related variables, suggesting that they reflect information beyond simply the location of an upcoming movement. Here, we examine the extent to which these representations arise from competitive spatial choice. We recorded SC activity in male mice performing a behavioral task requiring orienting movements to targets for a water reward in two contexts. In “competitive” trials, either the left or right target could be rewarded, depending on which stimulus was presented at the central port. In “noncompetitive” trials, the same target (e.g., left) was rewarded throughout an entire block. While both trial types required orienting movements to the same spatial targets, only in competitive trials do targets compete for selection. We found that in competitive trials, pre-movement SC activity predicted movement to contralateral targets, as expected. However, in noncompetitive trials, some neurons lost their spatial selectivity and in others activity predicted movement to ipsilateral targets. Consistent with these findings, unilateral optogenetic inactivation of pre-movement SC activity ipsiversively biased competitive, but not noncompetitive, trials. Incorporating these results into an attractor model of SC activity points to distinct pathways for orienting movements under competitive and noncompetitive conditions, with the SC specifically required for selecting among multiple potential targets.