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.
Background A continued effort in neuroscience aims to understand the way brain circuits consisting of diverse neuronal types generate complex behavior following sensory input. A common feature of vertebrate visual systems is that lower-order and higher-order visual areas are reciprocally connected. Feedforward projections confer visual responsiveness to higher-order visual neurons while feedback projections likely serve to modulate responses of lower-order visual neurons in a context-dependent manner. Optic tectum is the largest first-order visual brain area in zebrafish and is reciprocally connected with the torus longitudinalis (TL), a second-order visual brain area that does not receive retinal input. A functional role for feedback projections from TL to tectum has not been identified. Here we aim to understand how this feedback contributes to visual processing. Results In this study, we demonstrate that TL feedback projections to tectum drive binocular integration and spatial summation in a defined tectal circuit. We performed genetically targeted, cell type-specific functional imaging in tectal pyramidal neurons (PyrNs) and their two input neuron populations: retinal ganglion cells (RGCs) and neurons in TL. We find that PyrNs encode gradual changes in scene luminance using a complement of three distinct response classes that encode different light intensity ranges. Functional imaging of RGC inputs to tectum suggest that these response classes originate in the retina and RGC input specifies PyrN functional classes. In contrast, TL input serves to endow PyrNs with large, compound receptive fields that span both retinal hemifields. Conclusions These findings reveal a novel role for the zebrafish TL in driving binocular integration and spatial summation in tectal PyrNs. The neural circuit we describe generates a population of tectal neurons with large receptive fields tailored for detecting changes in the visual scene.
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