Identification of neurons in the superior colliculus that translate visual threat into sympathetic responses via a relay in the rostral ventromedial medulla

The superior colliculus (SC) is a sensory integration hub in the dorsal brainstem where multimodal information is combined and, depending on saliency of competing sensory inputs, appropriate motor commands and supportive autonomic changes initiated. In rodents, the SC is indispensable for initiating responses to stereotypical visual stimuli that resemble approaching objects (looming stimuli). In pilot experiments, we found that presentation of looming drove acute surges in blood pressure in telemetered conscious rats and that equivalent autonomic responses could be driven by complex visual stimuli (e.g. snakes) but not by control. Similar physiological responses were evoked by optogenetic SC stimulation in behaving animals, an effect that is at least partly mediated via a direct excitatory projection to the rostral ventromedial medulla (RVMM). We hypothesized that the encoding capabilities of the SC might extend beyond stereotypical approach, and that complex naturalistic shapes could be detected by SC circuits based on a saliency-map of relevant cues important for survival; resulting in the activation of acute autonomic effects when information is perceived as relevant. To investigate this, we made extracellular recordings of SC neurons (n >800 visually responsive neurons) in anaesthetized rats and used machine-learning to decode the visual cues presented. We found that SC circuits differentially encode different classes of visual stimuli, and that these tuning properties are present in opto-tagged SC neurons that project to the RVMM. Our data suggest that the SC is not only capable of nuanced object recognition, but can translate naturalistic visual cues into fast-acting autonomic changes.