UNLABELLED: Neurons respond to specific features of sensory stimuli. In the visual system, for example, some neurons respond to motion of small but not large objects, whereas other neurons prefer motion of the entire visual field. Separate neurons respond equally to local and global motion but selectively to additional features of visual stimuli. How and where does response selectivity emerge? Here, we show that wide-field (WF) cells in retino-recipient layers of the mouse superior colliculus (SC) respond selectively to small moving objects. Moreover, we identify two mechanisms that contribute to this selectivity. First, we show that input restricted to a small portion of the broad dendritic arbor of WF cells is sufficient to trigger dendritic spikes that reliably propagate to the soma/axon. In vivo whole-cell recordings reveal that nearly every action potential evoked by visual stimuli has characteristics of spikes initiated in dendrites. Second, inhibitory input from a different class of SC neuron, horizontal cells, constrains the range of stimuli to which WF cells respond. Horizontal cells respond preferentially to the sudden appearance or rapid movement of large stimuli. Optogenetic reduction of their activity reduces movement selectivity and broadens size tuning in WF cells by increasing the relative strength of responses to stimuli that appear suddenly or cover a large region of space. Therefore, strongly propagating dendritic spikes enable small stimuli to drive spike output in WF cells and local inhibition helps restrict responses to stimuli that are both small and moving.

SIGNIFICANCE STATEMENT: How do neurons respond selectively to some sensory stimuli but not others? In the visual system, a particularly relevant stimulus feature is object motion, which often reveals other animals. Here, we show how specific cells in the superior colliculus, one synapse downstream of the retina, respond selectively to object motion. These wide-field (WF) cells respond strongly to small objects that move slowly anywhere through a large region of space, but not to stationary objects or full-field motion. Action potential initiation in dendrites enables small stimuli to trigger visual responses and inhibitory input from cells that prefer large, suddenly appearing, or quickly moving stimuli restricts responses of WF cells to objects that are small and moving.

The mammalian retina conveys the vast majority of information about visual stimuli to two brain regions: the dorsal lateral geniculate nucleus (dLGN) and the superior colliculus (SC). The degree to which retinal ganglion cells (RGCs) send similar or distinct information to the two areas remains unclear despite the important constraints that different patterns of RGC input place on downstream visual processing. To resolve this ambiguity we injected a glycoprotein-deficient rabies virus coding for the expression of a fluorescent protein into the dLGN or SC; rabies virus labeled a smaller fraction of RGCs than lipophilic dyes like DiI but, crucially, did not label RGC axons of passage. ~80% of the RGCs infected by rabies virus injected into the dLGN were co-labeled with DiI injected into the SC, suggesting that many dLGN-projecting RGCs also project to the SC. However, functional characterization of RGCs revealed that the SC receives input from several classes of RGCs that largely avoid the dLGN - in particular, RGCs in which (1) sustained changes in light intensity elicit transient changes in firing rate and/or (2) a small range of stimulus sizes or temporal fluctuations in light intensity elicit robust activity. Taken together, our results illustrate several unexpected asymmetries in the information that the mouse retina conveys to two major downstream targets and suggest that differences in the output of dLGN and SC neurons reflect, at least in part, differences in the functional properties of RGCs that innervate the SC but not the dLGN.