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Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells.

ABSTRACT: Many neurons receive synapses in stereotypic proportions from converging but functionally distinct afferents. However, developmental mechanisms regulating synaptic convergence are not well understood. Here we describe a heterotypic mechanism by which one afferent controls synaptogenesis of another afferent, but not vice versa. Like other CNS circuits, zebrafish retinal H3 horizontal cells (HC) undergo an initial period of remodelling, establishing synapses with ultraviolet and blue cones while eliminating red and green cone contacts. As development progresses, the HCs selectively synapse with ultraviolet cones to generate a 5:1 ultraviolet-to-blue cone synapse ratio. Blue cone synaptogenesis increases in mutants lacking ultraviolet cones, and when transmitter release or visual stimulation of ultraviolet cones is perturbed. Connectivity is unaltered when blue cone transmission is suppressed. Moreover, there is no cell-autonomous regulation of cone synaptogenesis by neurotransmission. Thus, biased connectivity in this circuit is established by an unusual activity-dependent, unidirectional control of synaptogenesis exerted by the dominant input.

SUBMITTER: Yoshimatsu T

PROVIDER: S-EPMC4061492 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

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Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells.

Yoshimatsu Takeshi T Williams Philip R PR D'Orazi Florence D FD Suzuki Sachihiro C SC Fadool James M JM Allison W Ted WT Raymond Pamela A PA Wong Rachel O RO

Nature communications 20140515

Many neurons receive synapses in stereotypic proportions from converging but functionally distinct afferents. However, developmental mechanisms regulating synaptic convergence are not well understood. Here we describe a heterotypic mechanism by which one afferent controls synaptogenesis of another afferent, but not vice versa. Like other CNS circuits, zebrafish retinal H3 horizontal cells (HC) undergo an initial period of remodelling, establishing synapses with ultraviolet and blue cones while e ...[more]

PMID: 24832361

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Project description:Transcription factors have been implicated in the specification and differentiation of all cells in the mammalian retina with several transcription factors controlling the development of multiple neuronal subclasses. Horizontal cells and cone photoreceptors share a particularly intimate functional relationship but have been previously thought to develop through separate and distinct intrinsic molecular processes. We demonstrate that the zinc finger transcription factor Sall3 regulates development of both S-cone photoreceptors and horizontal cells. Our data shows that loss of function of Sall3 down-regulates the horizontal cell specific transcription factor Lhx1 and subsequently causes ectopic formation of horizontal-like wide-field amacrine cells partially phenocopying Lhx1-/- mice. Additionally, horizontal cells which laminate appropriately in Sall3 knockout mice show abnormal horizontal cell gene expression and failures in dendritic arborization. Over-expression of Sall3 also partially re-specifies cells to a horizontal-like wide-field amacrine fate. Intriguingly, Sall3 loss of function experiments also generated a massive reduction in the number of S-cone photoreceptors with remaining S-cones showing deficiencies in S-cone gene expression and morphology. Conversely, over-expression of Sall3 resulted in the ectopic expression of the S-cone specific genes S-opsin (Sop) and cone arrestin (Arr3) in electroporated cells. Our studies reveal that Sall3 regulates aspects of horizontal cell development in two ways: first, by maintaining Lhx1 expression, and second, by directly regulating expression of horizontal cell specific genes. We also show that Sall3 is an essential regulator of S-cone development in the mammalian retina and a potent activator of Sop and Arr3. Sall3 wild-type and knockout retinas used for explant cultures were extracted by microdissection at P0 in sterile PBS. Four cuts were made using micro-dissection scissors and the retinas were transferred to Nucleopore Track-Etch membrane filters (Whatman) and the tissue flattened out evenly. Filters were then floated on DMEM/F12, 10% FBS, 1X penicillin/streptomycin in 12 well plates and incubated at 37oC, 5% CO2 for 7 days. Three retinas (Sall3 knockout or wild-type) were pooled and RNA extracted using the Qiagen RNeasy kit. This was performed in triplicate for both wild-type and Sall3 knockouts retinas. A total of three replicates of Sall3 knockout and Sall3 wild-type RNA were analysed (six total samples).

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Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells.

Publications

Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells.

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