Superior colliculus projections drive dopamine neuron activity and movement but not value

To navigate complex environments, animals must rapidly integrate sensory information and respond appropriately to gather rewards and avoid threats. It is well established that dopamine neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) are key for creating and maintaining associations between environmental stimuli (i.e., cues) and the outcomes they predict, through Pavlovian learning. However, it remains unclear how relevant sensory information is integrated into dopamine (DA) pathways to guide exploration and learning. The superior colliculus (SC) receives direct visual input, and is anatomically positioned as a relay for rapid sensory augmentation of dopamine neurons, which could underlie the formation of Pavlovian associations. Here, we characterize the anatomical organization and functional impact of SC projections to the VTA and SNc in rats. First, using anatomical tracing techniques, we show that neurons in the intermediate and deep layers of SC synapse densely throughout the ventral midbrain, interfacing directly with neurons projecting to the striatum and ventral pallidum. Using fiber photometry, we find that these SC projections excite both dopamine and GABA neurons in the VTA and dopamine neurons in the SNc in vivo. Despite this, cues predicting SC terminal stimulation did not reliably evoke behavior on their own in an optogenetic Pavlovian conditioning paradigm. Further, optogenetic activation of SC terminals in the VTA/SNc did not support primary reinforcement or produce place preference or avoidance. Instead, we find that stimulation of SC terminals in the VTA and SNc reliably evoked head turning behavior. This body reorientation increased in intensity with repeated stimulations, suggesting that strengthening this circuit could underlie sensorimotor learning related to exploration and attentional bias. Together our results show that collicular neurons contribute to cueguided learning by controlling pose adjustments through interaction with dopamine systems.