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 dopamine pathways. The superior colliculus (SC) receives direct visual input and is positioned as a relay for dopamine neuron augmentation. We characterized the anatomical organization and functional impact of SC projections to the VTA and SNc in 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 dopamine 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 dopamine 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 dopamine neurons that preferentially engage movement instead of reward.