Superior Colliculus Projections Drive Dopamine Neuron Activity and Movement But Not Value

Abstract

To navigate dynamic environments, animals must rapidly integrate sensory information and respond appropriately to gather rewards and avoid threats. It is well established that dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SNc) are key for creating associations between environmental stimuli (i.e., cues) and the outcomes they predict. Critically, it remains unclear how sensory information is integrated into DA pathways. The superior colliculus (SC) receives direct visual input and is positioned as a relay for DA neuron augmentation. We characterized the anatomy and functional impact of SC projections to the VTA/SNc in male and female rats. First, we show that neurons in the deep layers of SC synapse densely throughout the ventral midbrain, interfacing with projections to the striatum and ventral pallidum, and these SC projections excite DA and GABA neurons in the VTA/SNc in vivo. Despite this, cues predicting SC→VTA/SNc neuron activation did not reliably evoke behavior in an optogenetic pavlovian conditioning paradigm, and activation of SC→VTA/SNc neurons did not support primary reinforcement or produce place preference/avoidance. Instead, we find that stimulation of SC→VTA/SNc neurons evokes head turning. Focusing optogenetic activation solely onto DA neurons that receive input from the SC was sufficient to invigorate turning, but not reinforcement. Turning intensity increased with repeated stimulations, suggesting that this circuit may underlie sensorimotor learning for exploration and attentional switching. Together, our results show that collicular neurons contribute to cue-guided behaviors by controlling pose adjustments through interaction with DA neurons that preferentially engage movement instead of reward.