Abstract
The torus longitudinalis (TL) is a midbrain structure unique to ray finned fish. Although previously implicated in orienting behaviors elicited by changes in ambient lighting, the role of TL in visual processing is not well-understood. TL is reciprocally connected to tectum and is the only known source of synaptic input to the stratum marginalis (SM) layer of tectal neuropil. Conversely, tectal pyramidal neurons (PyrNs) are the only identified tectal neuron population that forms a dendrite in SM. In this study we describe a zebrafish gal4 transgenic that labels TL neurons that project to SM. We demonstrate that the axonal TL projection to SM in zebrafish is glutamatergic. Consistent with these axons synapsing directly onto PyrNs, SM-targeted dendrites of PyrNs contain punctate enrichments of the glutamatergic post-synaptic marker protein PSD95. Sparse genetic labeling of individual TL axons and PyrN dendrites enabled quantitative morphometric analysis that revealed (1) large, sparsely branched TL axons in SM and (2) small, densely innervated PyrN dendrites in SM. Together this unique combination of morphologies support a wiring diagram in which TL inputs to PyrNs exhibit a high degree of convergence. We propose that this convergence functions to generate large, compound visual receptive fields in PyrNs. This quantitative anatomical data will instruct future functional studies aimed at identifying the precise contribution of TL-PyrN circuitry to visual behavior.
Highlights
The optic tectum is the largest visual brain area in zebrafish and is an important model system for examining the form and function of neural circuits mediating visually guided behavior
Single cell labeling of presynaptic torus longitudinalis (TL) neurons and post-synaptic pyramidal neuron (PyrN) enabled a detailed examination of how their morphologies constrain potential wiring diagrams
Our findings demonstrate that SM-projecting TL neuron (SMTL) axons are glutamatergic and PyrN dendrites in stratum marginalis (SM) contain glutamatergic post-synaptic specializations, direct evidence that SMTLs provide synaptic input to PyrNs in the larval zebrafish
Summary
The optic tectum is the largest visual brain area in zebrafish and is an important model system for examining the form and function of neural circuits mediating visually guided behavior. In addition to retinorecipient layers, this neuropil contains layers that receive input from other brain areas, including raphe nucleus, hypothalamus, and cerebellum (Heap et al, 2013, 2017; Filosa et al, 2016). Torus Longitudinalis Projections to Tectum tectal lobe is innervated by two non-retinorecipient brain areas that contain visually-responsive neurons, nucleus isthmi and torus longitudinalis (TL). Amphibians, and fish, the nucleus isthmi has been shown to mediate visual attention (Asadollahi et al, 2010, 2011; Marín et al, 2012) and recent findings suggest a similar role for nucleus isthmi in visually guided hunting behavior of larval zebrafish (Henriques et al, 2019). Less well-understood is the functional role of input from TL, a brain structure unique to ray-finned fish
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