A distinct circuit for biasing visual perceptual decisions and modulating superior colliculus activity through the mouse posterior striatum

Abstract

The basal ganglia play a key role in visual perceptual decisions. Despite being the primary target in the basal ganglia for inputs from the visual cortex, the posterior striatums (PS) involvement in visual perceptual behavior remains unknown in rodents. We reveal that the PS direct pathway is largely segregated from the dorsomedial striatum (DMS) direct pathway, the other major striatal target for visual cortex. We investigated the role of the PS in visual perceptual decisions by optogenetically stimulating striatal medium spiny neurons in the direct pathway (D1-MSNs) of mice performing a visual change-detection task. PS D1-MSN activation robustly biased visual decisions in a manner dependent on visual context, timing, and reward expectation. We examined the effects of PS and DMS direct pathway activation on neuronal activity in the superior colliculus (SC), a major output target of the basal ganglia. Activation of either direct pathway rapidly modulated SC neurons, but mostly targeted different SC neurons and had opposite effects. These results demonstrate that the PS in rodents provides an important route for controlling visual decisions, in parallel with the better known DMS, and with distinct anatomical and functional properties. Significance StatementThe rodent posterior striatum (PS) is strongly innervated by visual cortex and thalamus, but its functional role in visual behavior has not been explored. We show that the PS initiates a direct pathway through the basal ganglia that is anatomically distinct from the more commonly studied dorsomedial striatum (DMS). Activating the PS direct pathway selectively biases decisions for expected, valued visual events. We also show that both DMS and PS direct pathways modulate neuronal activity in the superior colliculus, a structure critical for visual processing and sensorimotor function, and preferentially modulate collicular units with properties relevant in the visual detection task. These findings identify a distinct and novel circuit through the basal ganglia for controlling visually guided perceptual decisions.