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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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Dynamic H3 HC processes selectively target UV cones(a,b) Multiphoton time-lapse imaging of an H3 HC in the background of (a) Tg(sws1:GFP) or (b) Tg(sws2:GFP). For each time point, an orthogonal view of the cell and labeled cones within the boxed region is provided below the connectivity map. A line-scan of this region showing the relative pixel intensities of the two channels (violet, UV cone signal or cyan, blue cone signal; yellow, HC signal) is presented below the view of the cell. Asterisks mark the location where, over time, a dendritic tip emerged and contacted UV or blue cones. Higher magnification of this location is shown on the right panels. A confocal reconstruction of the cell after fixation at the final time-point (104 hpf) clearly identifies the formation of new synapses. In the connectivity maps, solid circles represent synapses added in-between time points; open circles are stable contacts and X indicates eliminated contacts. Scale bars: 5 µm. (c) Population data showing the mean number of UV and blue cone synapses added and eliminated during the time course of multiphoton imaging. (d) Net change in the number of UV and blue cone synapses (n=5 for UV and n=3 for blue). Error bars are S.E.M.
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Figure 4: Dynamic H3 HC processes selectively target UV cones(a,b) Multiphoton time-lapse imaging of an H3 HC in the background of (a) Tg(sws1:GFP) or (b) Tg(sws2:GFP). For each time point, an orthogonal view of the cell and labeled cones within the boxed region is provided below the connectivity map. A line-scan of this region showing the relative pixel intensities of the two channels (violet, UV cone signal or cyan, blue cone signal; yellow, HC signal) is presented below the view of the cell. Asterisks mark the location where, over time, a dendritic tip emerged and contacted UV or blue cones. Higher magnification of this location is shown on the right panels. A confocal reconstruction of the cell after fixation at the final time-point (104 hpf) clearly identifies the formation of new synapses. In the connectivity maps, solid circles represent synapses added in-between time points; open circles are stable contacts and X indicates eliminated contacts. Scale bars: 5 µm. (c) Population data showing the mean number of UV and blue cone synapses added and eliminated during the time course of multiphoton imaging. (d) Net change in the number of UV and blue cone synapses (n=5 for UV and n=3 for blue). Error bars are S.E.M.

Mentions: The relatively constant number of blue cones contacted across ages may result from H3 HCs failing to attempt to form new synapses with this cone type after 3.5 dpf. Alternatively, H3 HCs may actively add contacts with blue cones after 3.5 dpf but eliminate these contacts. To distinguish between these possibilities, we performed timelapse imaging of H3 HCs in the background of labeled UV cones (Tg(sws1:GFP) or blue cones (Tg(sws2:GFP) for 24 hours, beginning at 3.5 dpf (Fig. 4). Throughout the period of imaging, UV cone contacts were both added and eliminated (Fig. 4a and c) but there was a net increase in the number of UV cones contacted by the end of the recording period (Fig. 4d). In contrast, H3 HCs only occasionally added or eliminated blue cone contacts (Fig. 4b and c), resulting in almost no net change in synapses with blue cones within this time period (Fig. 4d). In summary, within the 24 hour period of recording starting at 3.5 dpf, H3 HCs gained UV cone synapses, but no or relatively few blue cone contacts. Therefore, H3 HCs fail to increase their number of connections with blue cones over time because they do not actively engage blue cones in synaptogenesis after 3.5 dpf.


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)

Dynamic H3 HC processes selectively target UV cones(a,b) Multiphoton time-lapse imaging of an H3 HC in the background of (a) Tg(sws1:GFP) or (b) Tg(sws2:GFP). For each time point, an orthogonal view of the cell and labeled cones within the boxed region is provided below the connectivity map. A line-scan of this region showing the relative pixel intensities of the two channels (violet, UV cone signal or cyan, blue cone signal; yellow, HC signal) is presented below the view of the cell. Asterisks mark the location where, over time, a dendritic tip emerged and contacted UV or blue cones. Higher magnification of this location is shown on the right panels. A confocal reconstruction of the cell after fixation at the final time-point (104 hpf) clearly identifies the formation of new synapses. In the connectivity maps, solid circles represent synapses added in-between time points; open circles are stable contacts and X indicates eliminated contacts. Scale bars: 5 µm. (c) Population data showing the mean number of UV and blue cone synapses added and eliminated during the time course of multiphoton imaging. (d) Net change in the number of UV and blue cone synapses (n=5 for UV and n=3 for blue). Error bars are S.E.M.
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Figure 4: Dynamic H3 HC processes selectively target UV cones(a,b) Multiphoton time-lapse imaging of an H3 HC in the background of (a) Tg(sws1:GFP) or (b) Tg(sws2:GFP). For each time point, an orthogonal view of the cell and labeled cones within the boxed region is provided below the connectivity map. A line-scan of this region showing the relative pixel intensities of the two channels (violet, UV cone signal or cyan, blue cone signal; yellow, HC signal) is presented below the view of the cell. Asterisks mark the location where, over time, a dendritic tip emerged and contacted UV or blue cones. Higher magnification of this location is shown on the right panels. A confocal reconstruction of the cell after fixation at the final time-point (104 hpf) clearly identifies the formation of new synapses. In the connectivity maps, solid circles represent synapses added in-between time points; open circles are stable contacts and X indicates eliminated contacts. Scale bars: 5 µm. (c) Population data showing the mean number of UV and blue cone synapses added and eliminated during the time course of multiphoton imaging. (d) Net change in the number of UV and blue cone synapses (n=5 for UV and n=3 for blue). Error bars are S.E.M.
Mentions: The relatively constant number of blue cones contacted across ages may result from H3 HCs failing to attempt to form new synapses with this cone type after 3.5 dpf. Alternatively, H3 HCs may actively add contacts with blue cones after 3.5 dpf but eliminate these contacts. To distinguish between these possibilities, we performed timelapse imaging of H3 HCs in the background of labeled UV cones (Tg(sws1:GFP) or blue cones (Tg(sws2:GFP) for 24 hours, beginning at 3.5 dpf (Fig. 4). Throughout the period of imaging, UV cone contacts were both added and eliminated (Fig. 4a and c) but there was a net increase in the number of UV cones contacted by the end of the recording period (Fig. 4d). In contrast, H3 HCs only occasionally added or eliminated blue cone contacts (Fig. 4b and c), resulting in almost no net change in synapses with blue cones within this time period (Fig. 4d). In summary, within the 24 hour period of recording starting at 3.5 dpf, H3 HCs gained UV cone synapses, but no or relatively few blue cone contacts. Therefore, H3 HCs fail to increase their number of connections with blue cones over time because they do not actively engage blue cones in synaptogenesis after 3.5 dpf.

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