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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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Developmental increase in UV:blue cone synapse ratio occurs by selective addition of UV cone connections(a) Plots across ages of the mean ratio of the UV:blue cones available (circles) as well as the adjusted mean ratio of UV:blue cones that are contacted by H3 HCs (triangles). Contacted (n=6 for 3.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf); available (n=4 for all ages). (b) Mean H3 HC dendritic field sizes at different ages. (c) (Upper panel) Connectivity maps of example H3 HCs at different ages. A circle (yellow) with an area equivalent to the average 3.5 dpf H3 HC dendritic field size was centered on the center of mass of the dendritic field. (Lower panel) The mean numbers of UV and blue cone synapses within (In) or outside (Out) the yellow-filled circle were plotted for cells reconstructed at different ages. In general, synapses added outside the circle largely represent addition of synapses to the dendrites that grew after 3.5 dpf. In all panels, UV and blue cone synapse numbers obtained from FP expression in transgenic fish were adjusted according to the values of % transgenic expression per opsin expression from Supplementary Fig. 2. All error bars are S.E.M. p-values from Wilcoxon-Mann- Whitney rank sum test. n=6 for 3.5 dpf, n=9 for 5.5 dpf, n=8 for 10 dpf in (b,c).
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Figure 3: Developmental increase in UV:blue cone synapse ratio occurs by selective addition of UV cone connections(a) Plots across ages of the mean ratio of the UV:blue cones available (circles) as well as the adjusted mean ratio of UV:blue cones that are contacted by H3 HCs (triangles). Contacted (n=6 for 3.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf); available (n=4 for all ages). (b) Mean H3 HC dendritic field sizes at different ages. (c) (Upper panel) Connectivity maps of example H3 HCs at different ages. A circle (yellow) with an area equivalent to the average 3.5 dpf H3 HC dendritic field size was centered on the center of mass of the dendritic field. (Lower panel) The mean numbers of UV and blue cone synapses within (In) or outside (Out) the yellow-filled circle were plotted for cells reconstructed at different ages. In general, synapses added outside the circle largely represent addition of synapses to the dendrites that grew after 3.5 dpf. In all panels, UV and blue cone synapse numbers obtained from FP expression in transgenic fish were adjusted according to the values of % transgenic expression per opsin expression from Supplementary Fig. 2. All error bars are S.E.M. p-values from Wilcoxon-Mann- Whitney rank sum test. n=6 for 3.5 dpf, n=9 for 5.5 dpf, n=8 for 10 dpf in (b,c).

Mentions: The synaptic bias towards UV cones may be a consequence of a greater abundance of UV cones compared with blue cones in larval zebrafish23. We counted the number of UV cones and blue cones present within the retina from 3.5 to 10 dpf (Supplementary Fig. 2a,b), and compared these counts with the ratio of UV:blue cones that the H3 HC contacted (Fig. 3a). We found that the ratio of UV:blue cone synapses exceeds the relative abundance of UV and blue cones, suggesting that cone type ‘availability’ does not fully account for the biased connectivity with UV cones.


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)

Developmental increase in UV:blue cone synapse ratio occurs by selective addition of UV cone connections(a) Plots across ages of the mean ratio of the UV:blue cones available (circles) as well as the adjusted mean ratio of UV:blue cones that are contacted by H3 HCs (triangles). Contacted (n=6 for 3.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf); available (n=4 for all ages). (b) Mean H3 HC dendritic field sizes at different ages. (c) (Upper panel) Connectivity maps of example H3 HCs at different ages. A circle (yellow) with an area equivalent to the average 3.5 dpf H3 HC dendritic field size was centered on the center of mass of the dendritic field. (Lower panel) The mean numbers of UV and blue cone synapses within (In) or outside (Out) the yellow-filled circle were plotted for cells reconstructed at different ages. In general, synapses added outside the circle largely represent addition of synapses to the dendrites that grew after 3.5 dpf. In all panels, UV and blue cone synapse numbers obtained from FP expression in transgenic fish were adjusted according to the values of % transgenic expression per opsin expression from Supplementary Fig. 2. All error bars are S.E.M. p-values from Wilcoxon-Mann- Whitney rank sum test. n=6 for 3.5 dpf, n=9 for 5.5 dpf, n=8 for 10 dpf in (b,c).
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Figure 3: Developmental increase in UV:blue cone synapse ratio occurs by selective addition of UV cone connections(a) Plots across ages of the mean ratio of the UV:blue cones available (circles) as well as the adjusted mean ratio of UV:blue cones that are contacted by H3 HCs (triangles). Contacted (n=6 for 3.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf); available (n=4 for all ages). (b) Mean H3 HC dendritic field sizes at different ages. (c) (Upper panel) Connectivity maps of example H3 HCs at different ages. A circle (yellow) with an area equivalent to the average 3.5 dpf H3 HC dendritic field size was centered on the center of mass of the dendritic field. (Lower panel) The mean numbers of UV and blue cone synapses within (In) or outside (Out) the yellow-filled circle were plotted for cells reconstructed at different ages. In general, synapses added outside the circle largely represent addition of synapses to the dendrites that grew after 3.5 dpf. In all panels, UV and blue cone synapse numbers obtained from FP expression in transgenic fish were adjusted according to the values of % transgenic expression per opsin expression from Supplementary Fig. 2. All error bars are S.E.M. p-values from Wilcoxon-Mann- Whitney rank sum test. n=6 for 3.5 dpf, n=9 for 5.5 dpf, n=8 for 10 dpf in (b,c).
Mentions: The synaptic bias towards UV cones may be a consequence of a greater abundance of UV cones compared with blue cones in larval zebrafish23. We counted the number of UV cones and blue cones present within the retina from 3.5 to 10 dpf (Supplementary Fig. 2a,b), and compared these counts with the ratio of UV:blue cones that the H3 HC contacted (Fig. 3a). We found that the ratio of UV:blue cone synapses exceeds the relative abundance of UV and blue cones, suggesting that cone type ‘availability’ does not fully account for the biased connectivity with UV cones.

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