Visual field position shapes input sampling and output routing in the superior colliculus

Abstract

Animals use the location of visual stimuli to select appropriate actions1-5, and the upper and lower visual field often carry different ecological and behavioral meaning6-9. In mice, the superior colliculus is a key central hub that transforms visual input into orienting, defensive, and approach behaviors3,10-13. Its superficial layers receive retinotopically organized input from the retina and contain genetically defined cell types with distinct downstream projections, including wide-field neurons that project to the lateral posterior thalamus and narrow-field neurons that target the parabigeminal nucleus and deeper collicular layers14-18. These features raise the question of whether circuits of the superior colliculus are repeated across visual space or exhibit visual-field-dependent specializations. Here, we show that the mouse superficial superior colliculus contains visual-field-dependent circuit modules. Dual-color rabies tracing revealed that wide-field and narrow-field neurons receive input from a largely shared set of brain regions, whereas upper- and lower-field domains differ in how they sample those inputs. Some source regions preferentially innervate one visual-field domain, producing biased regional input strength, while others contain topographically segregated projecting neurons that target upper- or lower-field domains. MAPseq showed that most superficial collicular neurons project to single downstream targets, with upper- and lower-field populations differing in target probability. Two-photon calcium imaging further showed that wide-field neurons in upper- and lower-field domains differ in stimulus selectivity. Together, these findings reveal a visual-field-dependent wiring logic that biases how the superior colliculus samples inputs and routes signals to downstream pathways. HighlightsO_LIWide- and narrow-field neurons receive broadly overlapping inputs C_LIO_LIUpper- and lower-field domains differ in input strength and topographic organization C_LIO_LIMost superficial collicular neurons project to a single target C_LIO_LIVisual field position biases downstream target probability C_LI