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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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H3 HCs increase synaptogenesis with blue cones in the absence of UV cones(a–d) Maximum intensity projections of confocal image stacks of wholemount eyes in the background of Tg(sws1:GFP; sws2:mCherry). UV and blue cone distributions are shown for wildtype animals (a and b; control) and in the lor mutant (lor). Scale bars: 50 µm. (e–h) Example of an H3 HC visualized in lor, and its connectivity map. Inset in (e) shows a higher magnification view of enlarged dendritic tips within UV cones. Arrowheads in the orthogonal view of the cell (g,h) indicate dendritic tips invaginating blue cones. Scale bars: 5 µm. Note that in Figure 7, some UV cones in lor receive more than 1 dendritic invagination from the same HC. We counted these tips as a separate ‘synapse’. (i–l) Summary of mean measurements in control (ctr) and lor. See Methods for details of analysis. Each open circle represents one H3 HC. Error bars are S.E.M. p values from Wilcoxon-Mann-Whitney rank sum test.
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Figure 6: H3 HCs increase synaptogenesis with blue cones in the absence of UV cones(a–d) Maximum intensity projections of confocal image stacks of wholemount eyes in the background of Tg(sws1:GFP; sws2:mCherry). UV and blue cone distributions are shown for wildtype animals (a and b; control) and in the lor mutant (lor). Scale bars: 50 µm. (e–h) Example of an H3 HC visualized in lor, and its connectivity map. Inset in (e) shows a higher magnification view of enlarged dendritic tips within UV cones. Arrowheads in the orthogonal view of the cell (g,h) indicate dendritic tips invaginating blue cones. Scale bars: 5 µm. Note that in Figure 7, some UV cones in lor receive more than 1 dendritic invagination from the same HC. We counted these tips as a separate ‘synapse’. (i–l) Summary of mean measurements in control (ctr) and lor. See Methods for details of analysis. Each open circle represents one H3 HC. Error bars are S.E.M. p values from Wilcoxon-Mann-Whitney rank sum test.

Mentions: We next asked whether decreasing UV cone density during development would affect the H3 HC's connectivity pattern. We crossed the lor mutant, in which the total number of UV cones in the retina is reduced without changing the total number of blue cones25, into the background of the double transgenic, Tg(sws1:GFP; sws2:mCherry) (Fig. 6a–d). In the lor mutant, the few remaining UV cones appear in random patches across the retina (Fig. 6c). An example of an H3 HC and its connectivity pattern in the mutant at 5.5 dpf is provided in Figure 6e–h. There were no significant differences in H3 HC dendritic field size between the mutant and wildtype animals (Fig. 6i). However, H3 HCs increased contact with blue cones (Fig. 6k), resulting in only a small decrease in their total contact number compared with controls (Fig. 6j, k). H3 HCs thus contacted a significantly higher fraction of blue cones within their dendritic fields in the lor mutant (Fig. 6l).


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)

H3 HCs increase synaptogenesis with blue cones in the absence of UV cones(a–d) Maximum intensity projections of confocal image stacks of wholemount eyes in the background of Tg(sws1:GFP; sws2:mCherry). UV and blue cone distributions are shown for wildtype animals (a and b; control) and in the lor mutant (lor). Scale bars: 50 µm. (e–h) Example of an H3 HC visualized in lor, and its connectivity map. Inset in (e) shows a higher magnification view of enlarged dendritic tips within UV cones. Arrowheads in the orthogonal view of the cell (g,h) indicate dendritic tips invaginating blue cones. Scale bars: 5 µm. Note that in Figure 7, some UV cones in lor receive more than 1 dendritic invagination from the same HC. We counted these tips as a separate ‘synapse’. (i–l) Summary of mean measurements in control (ctr) and lor. See Methods for details of analysis. Each open circle represents one H3 HC. Error bars are S.E.M. p values from Wilcoxon-Mann-Whitney rank sum test.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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Figure 6: H3 HCs increase synaptogenesis with blue cones in the absence of UV cones(a–d) Maximum intensity projections of confocal image stacks of wholemount eyes in the background of Tg(sws1:GFP; sws2:mCherry). UV and blue cone distributions are shown for wildtype animals (a and b; control) and in the lor mutant (lor). Scale bars: 50 µm. (e–h) Example of an H3 HC visualized in lor, and its connectivity map. Inset in (e) shows a higher magnification view of enlarged dendritic tips within UV cones. Arrowheads in the orthogonal view of the cell (g,h) indicate dendritic tips invaginating blue cones. Scale bars: 5 µm. Note that in Figure 7, some UV cones in lor receive more than 1 dendritic invagination from the same HC. We counted these tips as a separate ‘synapse’. (i–l) Summary of mean measurements in control (ctr) and lor. See Methods for details of analysis. Each open circle represents one H3 HC. Error bars are S.E.M. p values from Wilcoxon-Mann-Whitney rank sum test.
Mentions: We next asked whether decreasing UV cone density during development would affect the H3 HC's connectivity pattern. We crossed the lor mutant, in which the total number of UV cones in the retina is reduced without changing the total number of blue cones25, into the background of the double transgenic, Tg(sws1:GFP; sws2:mCherry) (Fig. 6a–d). In the lor mutant, the few remaining UV cones appear in random patches across the retina (Fig. 6c). An example of an H3 HC and its connectivity pattern in the mutant at 5.5 dpf is provided in Figure 6e–h. There were no significant differences in H3 HC dendritic field size between the mutant and wildtype animals (Fig. 6i). However, H3 HCs increased contact with blue cones (Fig. 6k), resulting in only a small decrease in their total contact number compared with controls (Fig. 6j, k). H3 HCs thus contacted a significantly higher fraction of blue cones within their dendritic fields in the lor mutant (Fig. 6l).

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