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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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Inverse correlation between the number of UV and blue cones synapsing with H3 HCs in l or mutants(a,b) An example of an H3 HC labeled in Tg(sws1:GFP; sws2:mCherry) crossed in the lor background. Connectivity map is shown in (a). Arrowhead indicates an unusual invagination into a UV cone by two dendritic tips from the same HC. Dendritic tips of larval H3 HCs normally do not show such branching or co-innervation of the same pedicle. Scale bar: 5 µm. An inset shows High-magnification view of the tip indicated by the arrowhead. (c) Quantification of the mean number of dendritic tips invaginating a single UV cone in wildtype (ctr) and lor. Open circles represent the average value for individual H3 HCs. Error bars are S.E.M. (d) The number of blue and UV cones synapsing a given H3 HC (each circle) at 5.5 dpf are plotted here for wildtype (ctr) and lor mutants. All control H3 HCs had a single dendritic invagination into a cone pedicle. In lor, however, some H3 HCs project two or more dendritic tips into the cone pedicle (multiple tips). R-square and p-value from Pearson correlation coefficient.
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Figure 7: Inverse correlation between the number of UV and blue cones synapsing with H3 HCs in l or mutants(a,b) An example of an H3 HC labeled in Tg(sws1:GFP; sws2:mCherry) crossed in the lor background. Connectivity map is shown in (a). Arrowhead indicates an unusual invagination into a UV cone by two dendritic tips from the same HC. Dendritic tips of larval H3 HCs normally do not show such branching or co-innervation of the same pedicle. Scale bar: 5 µm. An inset shows High-magnification view of the tip indicated by the arrowhead. (c) Quantification of the mean number of dendritic tips invaginating a single UV cone in wildtype (ctr) and lor. Open circles represent the average value for individual H3 HCs. Error bars are S.E.M. (d) The number of blue and UV cones synapsing a given H3 HC (each circle) at 5.5 dpf are plotted here for wildtype (ctr) and lor mutants. All control H3 HCs had a single dendritic invagination into a cone pedicle. In lor, however, some H3 HCs project two or more dendritic tips into the cone pedicle (multiple tips). R-square and p-value from Pearson correlation coefficient.

Mentions: Like in wildtype, H3 HCs in lor contacted nearly 100% of the available UV cones, but each H3 HC in lor experienced variable densities of UV cones within their dendritic field. In some cells, the dendritic tips that invaginated UV cones were enlarged (Fig. 6e), whereas in other cases, H3 HCs projected two tips into the same UV cone (Fig. 7a–c). A plot of the number of UV cone versus blue cone synapses for individual cells in lor at 5.5 dpf (Fig. 7d) shows that in lor, there is an inverse relationship between the number of UV cones contacted and the number of blue cones contacted. Thus, H3 HCs respond to a lack of UV cones by modifying their dendritic contact area with available UV cones and by increasing their blue cone synapse number.


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)

Inverse correlation between the number of UV and blue cones synapsing with H3 HCs in l or mutants(a,b) An example of an H3 HC labeled in Tg(sws1:GFP; sws2:mCherry) crossed in the lor background. Connectivity map is shown in (a). Arrowhead indicates an unusual invagination into a UV cone by two dendritic tips from the same HC. Dendritic tips of larval H3 HCs normally do not show such branching or co-innervation of the same pedicle. Scale bar: 5 µm. An inset shows High-magnification view of the tip indicated by the arrowhead. (c) Quantification of the mean number of dendritic tips invaginating a single UV cone in wildtype (ctr) and lor. Open circles represent the average value for individual H3 HCs. Error bars are S.E.M. (d) The number of blue and UV cones synapsing a given H3 HC (each circle) at 5.5 dpf are plotted here for wildtype (ctr) and lor mutants. All control H3 HCs had a single dendritic invagination into a cone pedicle. In lor, however, some H3 HCs project two or more dendritic tips into the cone pedicle (multiple tips). R-square and p-value from Pearson correlation coefficient.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 7: Inverse correlation between the number of UV and blue cones synapsing with H3 HCs in l or mutants(a,b) An example of an H3 HC labeled in Tg(sws1:GFP; sws2:mCherry) crossed in the lor background. Connectivity map is shown in (a). Arrowhead indicates an unusual invagination into a UV cone by two dendritic tips from the same HC. Dendritic tips of larval H3 HCs normally do not show such branching or co-innervation of the same pedicle. Scale bar: 5 µm. An inset shows High-magnification view of the tip indicated by the arrowhead. (c) Quantification of the mean number of dendritic tips invaginating a single UV cone in wildtype (ctr) and lor. Open circles represent the average value for individual H3 HCs. Error bars are S.E.M. (d) The number of blue and UV cones synapsing a given H3 HC (each circle) at 5.5 dpf are plotted here for wildtype (ctr) and lor mutants. All control H3 HCs had a single dendritic invagination into a cone pedicle. In lor, however, some H3 HCs project two or more dendritic tips into the cone pedicle (multiple tips). R-square and p-value from Pearson correlation coefficient.
Mentions: Like in wildtype, H3 HCs in lor contacted nearly 100% of the available UV cones, but each H3 HC in lor experienced variable densities of UV cones within their dendritic field. In some cells, the dendritic tips that invaginated UV cones were enlarged (Fig. 6e), whereas in other cases, H3 HCs projected two tips into the same UV cone (Fig. 7a–c). A plot of the number of UV cone versus blue cone synapses for individual cells in lor at 5.5 dpf (Fig. 7d) shows that in lor, there is an inverse relationship between the number of UV cones contacted and the number of blue cones contacted. Thus, H3 HCs respond to a lack of UV cones by modifying their dendritic contact area with available UV cones and by increasing their blue cone synapse number.

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