Embodied Cognition and Decision-Making in the Primate Superior Colliculus

Abstract

A popular model of decision-making suggests that in primates, including humans, decisions evolve within forebrain structures responsible for preparing voluntary actions; a concert referred to as embodied cognition. Embodied cognition posits that in decision tasks, neuronal activity generally associated with preparing an action, actually reflects the accumulation of evidence for a particular decision. Testing the embodied cognition model causally is challenging because dissociating the evolution of a decision from preparing a motor act is difficult, if the same neuronal activity instantiates both processes. Ideally, one would show that manipulation of neuronal activity thought to be involved in movement preparation actually alters decisions, and not movement preparation. Here, trained monkeys performed a two-choice perceptual decision-making task in which they judged the orientation of a dynamic Glass pattern before and after unilateral, reversible inactivation of a brainstem area involved in preparing eye movements, the superior colliculus (SC). Surprisingly, we found that unilateral SC inactivation produced significant decision biases and changes in reaction times consistent with a role for the SC in evidence accumulation. Fitting signal detection theory and sequential sampling models (drift-diffusion and urgency-gating) to the data revealed that SC inactivation produced a decrease in the relative evidence for contralateral decisions. Control experiments showed that SC inactivation did not result in eye movement biases ruling out interpretations based on motor preparation or spatial attentional impairment. The results provide causal evidence for an embodied cognition model of perceptual decision-making and provide compelling evidence that the SC of primates plays a causal role in modulating evidence accumulation for perceptual decisions, a process that is usually attributed to the cerebral cortex.

Unraveling circuits of visual perception and cognition through the superior colliculus

“…Importantly, in this experiment, monkeys also performed a saccade selection task in which they made saccades to the same two locations as the choice targets, but neither perceptual ambiguity nor orientation discrimination occurred. Here, muscimol did not impair the monkeys' ability to distribute their saccadic choices equally between the two locations, ruling out interpretations based on motor or attentional biases (Jun et al, 2020). An extensive modeling effort revealed that muscimol inactivation produced a decrease in the relative evidence for decisions made to the inactivated field (Jun et al, 2020), consistent with previous modeling efforts in the SC (e.g., Ratcliff et al, 2003Ratcliff et al, , 2007.…”

“…Here, muscimol did not impair the monkeys' ability to distribute their saccadic choices equally between the two locations, ruling out interpretations based on motor or attentional biases (Jun et al, 2020). An extensive modeling effort revealed that muscimol inactivation produced a decrease in the relative evidence for decisions made to the inactivated field (Jun et al, 2020), consistent with previous modeling efforts in the SC (e.g., Ratcliff et al, 2003Ratcliff et al, , 2007. Interestingly, inactivation of cortical area LIP showed impairments only in sensory aspects of decisions and not in decision-making per se (Katz et al, 2016;Zhou and Freedman, 2019).…”