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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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Connectivity patterns of H3 HCs across development(a) Examples of larval H3 HCs transiently expressing fluorescent protein in the background of Tg(sws1:GFP; sws2:mCherry). Shown are maximum intensity projections or orthogonal views through a small part of the arbor. Insets in top view panels show higher magnifications of dendritic tips invaginating into a cone pedicle. Open circles map the locations of dendritic tips that contacted UV or blue cones in the double transgenic line (magenta or blue circles respectively), as judged from 3D reconstructions of the cell and its surrounding cones. Some tips (orange circles, undefined) could not be assigned to either UV or blue cones. Scale bars: 5 µm. (b) Population data showing the mean number of UV or blue cone-associated tips and undefined tips made by H3 HCs in the background of Tg(sws1:GFP; sws2:mCherry) fish. Each open circle represents one cell. n=6 for 3.5 dpf, n=9 for 4.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf. Error bars are S.E.M.
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Figure 2: Connectivity patterns of H3 HCs across development(a) Examples of larval H3 HCs transiently expressing fluorescent protein in the background of Tg(sws1:GFP; sws2:mCherry). Shown are maximum intensity projections or orthogonal views through a small part of the arbor. Insets in top view panels show higher magnifications of dendritic tips invaginating into a cone pedicle. Open circles map the locations of dendritic tips that contacted UV or blue cones in the double transgenic line (magenta or blue circles respectively), as judged from 3D reconstructions of the cell and its surrounding cones. Some tips (orange circles, undefined) could not be assigned to either UV or blue cones. Scale bars: 5 µm. (b) Population data showing the mean number of UV or blue cone-associated tips and undefined tips made by H3 HCs in the background of Tg(sws1:GFP; sws2:mCherry) fish. Each open circle represents one cell. n=6 for 3.5 dpf, n=9 for 4.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf. Error bars are S.E.M.

Mentions: Adult H3 HCs only contact UV and blue cones16, but whether H3 HCs also demonstrate this wiring specificity during development is not known. In order to obtain the connectivity patterns of developing H3 HCs, we coinjected pCx55.5:Gal4 and pUAS:MXFP plasmids into double transgenic fish in which UV cones (sws1:GFP) and blue cones (sws2:mCherry) express different color fluorescent proteins (FP) under cone type-specific promoters. We obtained confocal reconstructions of H3 HCs at various larval ages, from 3.5 days postfertilization (dpf), around the onset of synaptogenesis in the outer plexiform layer (OPL)20, to 10.5 dpf, when visually guided behavior is well-established21 (Fig. 2a). At all ages studied, H3 HCs contacted mostly UV and blue cones (Fig. 2b). On average, the number of UV cones contacted by an H3 HC increased with age (p<0.01; one-way ANOVA), whereas the number of blue cone synapses remained constant across time points (p>0.05; one-way ANOVA) (Fig. 2b).


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)

Connectivity patterns of H3 HCs across development(a) Examples of larval H3 HCs transiently expressing fluorescent protein in the background of Tg(sws1:GFP; sws2:mCherry). Shown are maximum intensity projections or orthogonal views through a small part of the arbor. Insets in top view panels show higher magnifications of dendritic tips invaginating into a cone pedicle. Open circles map the locations of dendritic tips that contacted UV or blue cones in the double transgenic line (magenta or blue circles respectively), as judged from 3D reconstructions of the cell and its surrounding cones. Some tips (orange circles, undefined) could not be assigned to either UV or blue cones. Scale bars: 5 µm. (b) Population data showing the mean number of UV or blue cone-associated tips and undefined tips made by H3 HCs in the background of Tg(sws1:GFP; sws2:mCherry) fish. Each open circle represents one cell. n=6 for 3.5 dpf, n=9 for 4.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf. Error bars are S.E.M.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4061492&req=5

Figure 2: Connectivity patterns of H3 HCs across development(a) Examples of larval H3 HCs transiently expressing fluorescent protein in the background of Tg(sws1:GFP; sws2:mCherry). Shown are maximum intensity projections or orthogonal views through a small part of the arbor. Insets in top view panels show higher magnifications of dendritic tips invaginating into a cone pedicle. Open circles map the locations of dendritic tips that contacted UV or blue cones in the double transgenic line (magenta or blue circles respectively), as judged from 3D reconstructions of the cell and its surrounding cones. Some tips (orange circles, undefined) could not be assigned to either UV or blue cones. Scale bars: 5 µm. (b) Population data showing the mean number of UV or blue cone-associated tips and undefined tips made by H3 HCs in the background of Tg(sws1:GFP; sws2:mCherry) fish. Each open circle represents one cell. n=6 for 3.5 dpf, n=9 for 4.5 dpf, n=12 for 5.5 dpf, n=8 for 10 dpf. Error bars are S.E.M.
Mentions: Adult H3 HCs only contact UV and blue cones16, but whether H3 HCs also demonstrate this wiring specificity during development is not known. In order to obtain the connectivity patterns of developing H3 HCs, we coinjected pCx55.5:Gal4 and pUAS:MXFP plasmids into double transgenic fish in which UV cones (sws1:GFP) and blue cones (sws2:mCherry) express different color fluorescent proteins (FP) under cone type-specific promoters. We obtained confocal reconstructions of H3 HCs at various larval ages, from 3.5 days postfertilization (dpf), around the onset of synaptogenesis in the outer plexiform layer (OPL)20, to 10.5 dpf, when visually guided behavior is well-established21 (Fig. 2a). At all ages studied, H3 HCs contacted mostly UV and blue cones (Fig. 2b). On average, the number of UV cones contacted by an H3 HC increased with age (p<0.01; one-way ANOVA), whereas the number of blue cone synapses remained constant across time points (p>0.05; one-way ANOVA) (Fig. 2b).

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