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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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UV cone transmission regulates blue cone synapse number(a–l) Examples of H3 HCs and their connectivity maps in the background of Tg(sws1:TeNT; sws2:mCherry) (a-d), Tg(sws1:GFP; sws2:TeNT) (e–h), or Tg(sws1:TeNT; sws2:TeNT; sws2:mCherry) (i–l). Sideviews of rectangular regions outlined in (a,e,i) are shown in (c,d,g,h,k,l). Arrowheads indicate blue cone synapses. Scale bars: 5 µm. (m–o) Comparison of mean measurements across conditions. See Methods for details of analysis. Control animals (ctr). 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 8: UV cone transmission regulates blue cone synapse number(a–l) Examples of H3 HCs and their connectivity maps in the background of Tg(sws1:TeNT; sws2:mCherry) (a-d), Tg(sws1:GFP; sws2:TeNT) (e–h), or Tg(sws1:TeNT; sws2:TeNT; sws2:mCherry) (i–l). Sideviews of rectangular regions outlined in (a,e,i) are shown in (c,d,g,h,k,l). Arrowheads indicate blue cone synapses. Scale bars: 5 µm. (m–o) Comparison of mean measurements across conditions. See Methods for details of analysis. Control animals (ctr). Each open circle represents one H3 HC. Error bars are S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test.

Mentions: Our finding of a compensatory increase in blue cone contacts in the lor mutant suggests that the H3 HC’s dominant partner type, UV cones, influence connectivity with the secondary partner type, blue cones. Is this regulation mediated by transmission from cones? To test this possibility, we generated transgenic fish in which tetanus toxin fused to cyan fluorescent protein (TeNT-CFP) is expressed in UV, blue, or both cone types, without changing their densities (Supplementary Fig. 5a). TeNT perturbs exocytosis26 and thus reduces synaptic transmission. Figure 8a–l shows an example of an H3 HC and its connectivity pattern at 5.5 dpf from each of the TeNT transgenic lines. Reduction in transmission from UV, blue, or both cone types did not affect the dendritic field size of H3 HCs relative to controls (Fig. 8m).


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)

UV cone transmission regulates blue cone synapse number(a–l) Examples of H3 HCs and their connectivity maps in the background of Tg(sws1:TeNT; sws2:mCherry) (a-d), Tg(sws1:GFP; sws2:TeNT) (e–h), or Tg(sws1:TeNT; sws2:TeNT; sws2:mCherry) (i–l). Sideviews of rectangular regions outlined in (a,e,i) are shown in (c,d,g,h,k,l). Arrowheads indicate blue cone synapses. Scale bars: 5 µm. (m–o) Comparison of mean measurements across conditions. See Methods for details of analysis. Control animals (ctr). 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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getmorefigures.php?uid=PMC4061492&req=5

Figure 8: UV cone transmission regulates blue cone synapse number(a–l) Examples of H3 HCs and their connectivity maps in the background of Tg(sws1:TeNT; sws2:mCherry) (a-d), Tg(sws1:GFP; sws2:TeNT) (e–h), or Tg(sws1:TeNT; sws2:TeNT; sws2:mCherry) (i–l). Sideviews of rectangular regions outlined in (a,e,i) are shown in (c,d,g,h,k,l). Arrowheads indicate blue cone synapses. Scale bars: 5 µm. (m–o) Comparison of mean measurements across conditions. See Methods for details of analysis. Control animals (ctr). Each open circle represents one H3 HC. Error bars are S.E.M. p-values from Wilcoxon-Mann-Whitney rank sum test.
Mentions: Our finding of a compensatory increase in blue cone contacts in the lor mutant suggests that the H3 HC’s dominant partner type, UV cones, influence connectivity with the secondary partner type, blue cones. Is this regulation mediated by transmission from cones? To test this possibility, we generated transgenic fish in which tetanus toxin fused to cyan fluorescent protein (TeNT-CFP) is expressed in UV, blue, or both cone types, without changing their densities (Supplementary Fig. 5a). TeNT perturbs exocytosis26 and thus reduces synaptic transmission. Figure 8a–l shows an example of an H3 HC and its connectivity pattern at 5.5 dpf from each of the TeNT transgenic lines. Reduction in transmission from UV, blue, or both cone types did not affect the dendritic field size of H3 HCs relative to controls (Fig. 8m).

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