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The zebrafish visual system transmits dimming information via multiple segregated pathways

Vertebrate retinas contain circuits specialized to encode light level decrements. This information is transmitted to the brain by dimming‐sensitive OFF retinal ganglion cells (OFF‐RGCs) that respond to light decrements with increased firing. It is known that OFF‐RGCs with distinct photosensitivity profiles form parallel visual channels to the vertebrate brain, yet how these channels are processed by first‐ and higher order brain areas has not been well characterized in any species. To address this question in the larval zebrafish visual system, we examined the visual response properties of a genetically identified population of tectal neurons with a defined axonal projection to a second‐order visual area: id2b:gal4‐positive torus longitudinalis projection neurons (TLPNs). TLPNs responded consistently to whole‐field dimming stimuli and exhibited the strongest responses when dimming was preceded by low light levels. Functional characterization of OFF‐RGC terminals in tectum revealed responses that varied in their photosensitivities: (a) low‐sensitivity OFF‐RGCs that selectively respond to large light decrements, (b) high‐sensitivity OFF‐RGCs that selectively encode small decrements, and (c) broad sensitivity OFF‐RGCs that respond to a wide range of light decrements. Diverse photosensitivity profiles were also observed using pan‐neuronal calcium imaging to identify dimming‐responsive neurons in both tectum and torus longitudinalis. Together, these data support a model in which parallel OFF channels generated in the retina remain segregated across three stages of visual processing. Segregated OFF channels with different sensitivities may allow specific aspects of dimming‐evoked behaviors to be modulated by ambient light levels.