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

Yoshimatsu T, Williams PR, D'Orazi FD, Suzuki SC, Fadool JM, Allison WT, Raymond PA, Wong RO - Nat Commun (2014)

Bottom Line: As development progresses, the HCs selectively synapse with ultraviolet cones to generate a 5:1 ultraviolet-to-blue cone synapse ratio.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.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biological Structure, University of Washington, 1959 NE Pacific Street, Seattle, Washington 98195, USA [2].

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.

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Morphology of HCs in larval zebrafish retina(a) Examples of HCs at 3.5 days postfertilization (dpf) visualized by injecting plasmid DNA (see Methods for details) into fertilized eggs. Shown here is the maximum intensity projection of a confocal image stack of the back of an isolated eye. (b,c) Orthogonal views of two-photon reconstructions of cone HCs in live fish (3.5 dpf). Dendritic tips extending from the HCs are clearly visible from these side views. Scale bars (a–c): 5 µm. (d) Tip density plotted against dendritic field size of morphologically classified H1/2 and H3 HCs at 3.5 dpf. The dendritic field is defined as the area encompassed by a convex polygon whose corners touch the outer most dendritic tips. Each open or gray symbol represents a cell. Black symbols and error bars represent means and S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test. n=9 for H1/2 and n=6 for H3. (e) EM image of a cone pedicle showing invaginating HC dendritic tips (red) that are apposed to characteristic pre-synaptic ribbons, sites of transmitter release (arrows). (f) Single plane confocal image showing Gria2/3 (also known as GluR2/3) immunoreactive puncta (green) colocalized with a HC dendritic tip (red) within a cone pedicle (blue). Scale bar (e,f): 0.5 µm.
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Figure 1: Morphology of HCs in larval zebrafish retina(a) Examples of HCs at 3.5 days postfertilization (dpf) visualized by injecting plasmid DNA (see Methods for details) into fertilized eggs. Shown here is the maximum intensity projection of a confocal image stack of the back of an isolated eye. (b,c) Orthogonal views of two-photon reconstructions of cone HCs in live fish (3.5 dpf). Dendritic tips extending from the HCs are clearly visible from these side views. Scale bars (a–c): 5 µm. (d) Tip density plotted against dendritic field size of morphologically classified H1/2 and H3 HCs at 3.5 dpf. The dendritic field is defined as the area encompassed by a convex polygon whose corners touch the outer most dendritic tips. Each open or gray symbol represents a cell. Black symbols and error bars represent means and S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test. n=9 for H1/2 and n=6 for H3. (e) EM image of a cone pedicle showing invaginating HC dendritic tips (red) that are apposed to characteristic pre-synaptic ribbons, sites of transmitter release (arrows). (f) Single plane confocal image showing Gria2/3 (also known as GluR2/3) immunoreactive puncta (green) colocalized with a HC dendritic tip (red) within a cone pedicle (blue). Scale bar (e,f): 0.5 µm.

Mentions: HCs in zebrafish larval retina were labeled by expression of fluorescent protein under the Cx55.5 promoter18 (Fig. 1a–c). As in adult zebrafish15, H1 and H2 (H1/2) cone HCs in larvae could not be readily distinguished from each other by their dendritic morphology alone, whereas H1/2 and H3 HCs appeared morphologically distinct (Fig. 1a–c). We found that shortly after HC genesis, H3 HCs showed lower densities of dendritic tips and larger dendritic field sizes than H1/2 HCs (Fig. 1d). These morphological differences persisted in older larvae (Supplementary Fig. 1). As in adult zebrafish, we observed that larval HCs made invaginating dendritic contacts with cone photoreceptor axonal terminals, or pedicles. The dendritic tips of the HCs were apposed to presynaptic ribbon structures (Fig. 1e), and contained ionotropic glutamate receptors (Fig. 1f) as previously demonstrated19. We define here an HC-cone synapse as the invagination of a single dendritic tip within an individual cone pedicle.


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

Yoshimatsu T, Williams PR, D'Orazi FD, Suzuki SC, Fadool JM, Allison WT, Raymond PA, Wong RO - Nat Commun (2014)

Morphology of HCs in larval zebrafish retina(a) Examples of HCs at 3.5 days postfertilization (dpf) visualized by injecting plasmid DNA (see Methods for details) into fertilized eggs. Shown here is the maximum intensity projection of a confocal image stack of the back of an isolated eye. (b,c) Orthogonal views of two-photon reconstructions of cone HCs in live fish (3.5 dpf). Dendritic tips extending from the HCs are clearly visible from these side views. Scale bars (a–c): 5 µm. (d) Tip density plotted against dendritic field size of morphologically classified H1/2 and H3 HCs at 3.5 dpf. The dendritic field is defined as the area encompassed by a convex polygon whose corners touch the outer most dendritic tips. Each open or gray symbol represents a cell. Black symbols and error bars represent means and S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test. n=9 for H1/2 and n=6 for H3. (e) EM image of a cone pedicle showing invaginating HC dendritic tips (red) that are apposed to characteristic pre-synaptic ribbons, sites of transmitter release (arrows). (f) Single plane confocal image showing Gria2/3 (also known as GluR2/3) immunoreactive puncta (green) colocalized with a HC dendritic tip (red) within a cone pedicle (blue). Scale bar (e,f): 0.5 µm.
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Related In: Results  -  Collection

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Figure 1: Morphology of HCs in larval zebrafish retina(a) Examples of HCs at 3.5 days postfertilization (dpf) visualized by injecting plasmid DNA (see Methods for details) into fertilized eggs. Shown here is the maximum intensity projection of a confocal image stack of the back of an isolated eye. (b,c) Orthogonal views of two-photon reconstructions of cone HCs in live fish (3.5 dpf). Dendritic tips extending from the HCs are clearly visible from these side views. Scale bars (a–c): 5 µm. (d) Tip density plotted against dendritic field size of morphologically classified H1/2 and H3 HCs at 3.5 dpf. The dendritic field is defined as the area encompassed by a convex polygon whose corners touch the outer most dendritic tips. Each open or gray symbol represents a cell. Black symbols and error bars represent means and S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test. n=9 for H1/2 and n=6 for H3. (e) EM image of a cone pedicle showing invaginating HC dendritic tips (red) that are apposed to characteristic pre-synaptic ribbons, sites of transmitter release (arrows). (f) Single plane confocal image showing Gria2/3 (also known as GluR2/3) immunoreactive puncta (green) colocalized with a HC dendritic tip (red) within a cone pedicle (blue). Scale bar (e,f): 0.5 µm.
Mentions: HCs in zebrafish larval retina were labeled by expression of fluorescent protein under the Cx55.5 promoter18 (Fig. 1a–c). As in adult zebrafish15, H1 and H2 (H1/2) cone HCs in larvae could not be readily distinguished from each other by their dendritic morphology alone, whereas H1/2 and H3 HCs appeared morphologically distinct (Fig. 1a–c). We found that shortly after HC genesis, H3 HCs showed lower densities of dendritic tips and larger dendritic field sizes than H1/2 HCs (Fig. 1d). These morphological differences persisted in older larvae (Supplementary Fig. 1). As in adult zebrafish, we observed that larval HCs made invaginating dendritic contacts with cone photoreceptor axonal terminals, or pedicles. The dendritic tips of the HCs were apposed to presynaptic ribbon structures (Fig. 1e), and contained ionotropic glutamate receptors (Fig. 1f) as previously demonstrated19. We define here an HC-cone synapse as the invagination of a single dendritic tip within an individual cone pedicle.

Bottom Line: As development progresses, the HCs selectively synapse with ultraviolet cones to generate a 5:1 ultraviolet-to-blue cone synapse ratio.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.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biological Structure, University of Washington, 1959 NE Pacific Street, Seattle, Washington 98195, USA [2].

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.

Show MeSH
Related in: MedlinePlus