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.