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

Abstract

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

Inhibitory midbrain neurons mediate decision making

“…neurons: 49/72; Ipsi. neurons = 23/72; p = 0.0022, Χ 2 test), consistent with previous results [11][12][13] . Within the population of GABAergic neurons, we also found that more neurons preferred the contralateral than the ipsilateral choice ( Fig.…”

“…When the sensory evidence for the rewarded choice is strong (i.e., on easy trials), input from upstream regions may dominate processing in the SC (or outweigh SC contributions at downstream circuits in the brainstem). Conversely, when the sensory evidence is weak (i.e., on difficult trials), intrinsic SC processing, including via the GABAergic SC neurons studied here, may have more weight in determining the output of competing choices and therefore exert a stronger influence over spatial choice 13 .…”

“…Elucidating the roles of specific cell types in decision making is a critical step toward understanding functional neural circuits and biologically plausible theoretical frameworks for decisions. In this study, we leveraged behavioral, optogenetic, electrophysiological and computational approaches to identify the functional role of inhibitory neurons in the SC in spatial choice, an important and tractable form of decision making for which the SC plays a critical role conserved across species 7,13 . We initially hypothesized that GABAergic SC neurons function to locally inhibit glutamatergic output representing contralateral choices ( Fig.…”

“…Given that SC activity represents contralateral targets 8,11,41 , including in mice performing this task 13 , we predicted that activating GABAergic SC neurons would inhibit nearby neurons representing the contralateral choice and therefore bias choices ipsilaterally ( Fig. 1a,d).…”

“…Spatial choiceselecting where to attend or to moveis ideal for this purpose: it is an adaptive form of decision making that is critical for survival, and several lines of evidence, across primates, cats and rodents, implicate the intermediate and deep layers of the midbrain superior colliculus (SC) in this function [7][8][9] . Targets in contralateral space are represented in the SC earlier than in other choice-related brain regions [10][11][12][13][14][15] , and manipulating SC activity during choice produces predictable choice biases [15][16][17][18][19][20] . These and other data showing that SC activity reflects target value and other decision-related variables 12,21,22 demonstrate that the SC, traditionally appreciated for initiating orienting motor commands, is required for choosing where to move 7 .…”