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Developmental patterning of glutamatergic synapses onto retinal ganglion cells.

Morgan JL, Schubert T, Wong RO - Neural Dev (2008)

Bottom Line: We found that as dendritic density (dendritic length per unit area of dendritic field) decreases with maturation, the density of synapses along the dendrites increases.The spatial pattern of glutamatergic inputs onto RGCs arises early in synaptogenesis despite ensuing reorganization of dendritic structure.We raise the possibility that these early patterns of synaptic distributions may arise from constraints placed on the number of contacts presynaptic neurons are able to make with the RGCs.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Structure, University of Washington, Seattle, WA 98195, USA. j37@u.washington.edu

ABSTRACT

Background: Neurons receive excitatory synaptic inputs that are distributed across their dendritic arbors at densities and with spatial patterns that influence their output. How specific synaptic distributions are attained during development is not well understood. The distribution of glutamatergic inputs across the dendritic arbors of mammalian retinal ganglion cells (RGCs) has long been correlated to the spatial receptive field profiles of these neurons. Thus, determining how glutamatergic inputs are patterned onto RGC dendritic arbors during development could provide insight into the cellular mechanisms that shape their functional receptive fields.

Results: We transfected developing and mature mouse RGCs with plasmids encoding fluorescent proteins that label their dendrites and glutamatergic postsynaptic sites. We found that as dendritic density (dendritic length per unit area of dendritic field) decreases with maturation, the density of synapses along the dendrites increases. These changes appear coordinated such that RGCs attain the mature average density of postsynaptic sites per unit area (areal density) by the time synaptic function emerges. Furthermore, stereotypic centro-peripheral gradients in the areal density of synapses across the arbor of RGCs are established at an early developmental stage.

Conclusion: The spatial pattern of glutamatergic inputs onto RGCs arises early in synaptogenesis despite ensuing reorganization of dendritic structure. We raise the possibility that these early patterns of synaptic distributions may arise from constraints placed on the number of contacts presynaptic neurons are able to make with the RGCs.

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Comparison of ON and OFF arbors of bistratified cells across development. (a-c) Global dendritic and puncta densities for bistratified and P5 RGCs. ON arbors are shown in green. OFF arbors are shown in red. Error bars = standard error of mean. (d-f) Ratio of dendritic and puncta densities of the inner half of the dendritic arbor divided by the outer half. (g) Scatter plot comparing areal density of puncta between ON and OFF arbors of individual cells for all ages recorded. (h) Scatter plots showing the relationship of differences in P/A and D/A between the ON and OFF arbors. ΔP/A = [P/AON - P/AOFF]/[P/AON + P/AOFF]. Similar calculations were obtained for D/A (ΔD/A). R = correlation of coefficient. P-values indicate the probability of producing the given R-value from a random pairing of the data.
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Figure 8: Comparison of ON and OFF arbors of bistratified cells across development. (a-c) Global dendritic and puncta densities for bistratified and P5 RGCs. ON arbors are shown in green. OFF arbors are shown in red. Error bars = standard error of mean. (d-f) Ratio of dendritic and puncta densities of the inner half of the dendritic arbor divided by the outer half. (g) Scatter plot comparing areal density of puncta between ON and OFF arbors of individual cells for all ages recorded. (h) Scatter plots showing the relationship of differences in P/A and D/A between the ON and OFF arbors. ΔP/A = [P/AON - P/AOFF]/[P/AON + P/AOFF]. Similar calculations were obtained for D/A (ΔD/A). R = correlation of coefficient. P-values indicate the probability of producing the given R-value from a random pairing of the data.

Mentions: Our analysis thus far has focused on the synaptic distributions of monostratified cells across development, which is likely to include more than one type of RGC. Bistratified cells, however, provide an opportunity for us to compare the dendritic and synaptic fields of two dendritic arbors within the same cell. To separate the ON and OFF arbors of a bistratified cell, each cell was digitally rotated so that its arbors were orthogonal to the z dimension. We then plotted the distribution of dendritic length along the z dimension and identified the division between ON and OFF arbors by the trough between the two peaks. Dendritic density, areal synaptic density and linear synaptic density are plotted for the ON and OFF arbors of each bistratified cell at various ages in Figure 8. Overall, both the ON and OFF arbors of bistratified cells appeared to follow the same developmental patterns as monostratified cells, although the changes in D/A and P/D were not as pronounced (Figure 8a–f). Bistratified cells, however, exhibited a shallower centro-peripheral gradient compared to monostratified cells: from P7 onwards, the gradient in areal puncta density was significantly lower in the arbors of bistratified cells (1.66 ± 0.10), compared to monostratified cells (1.91 ± 0.08; P = 0.015).


Developmental patterning of glutamatergic synapses onto retinal ganglion cells.

Morgan JL, Schubert T, Wong RO - Neural Dev (2008)

Comparison of ON and OFF arbors of bistratified cells across development. (a-c) Global dendritic and puncta densities for bistratified and P5 RGCs. ON arbors are shown in green. OFF arbors are shown in red. Error bars = standard error of mean. (d-f) Ratio of dendritic and puncta densities of the inner half of the dendritic arbor divided by the outer half. (g) Scatter plot comparing areal density of puncta between ON and OFF arbors of individual cells for all ages recorded. (h) Scatter plots showing the relationship of differences in P/A and D/A between the ON and OFF arbors. ΔP/A = [P/AON - P/AOFF]/[P/AON + P/AOFF]. Similar calculations were obtained for D/A (ΔD/A). R = correlation of coefficient. P-values indicate the probability of producing the given R-value from a random pairing of the data.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2311295&req=5

Figure 8: Comparison of ON and OFF arbors of bistratified cells across development. (a-c) Global dendritic and puncta densities for bistratified and P5 RGCs. ON arbors are shown in green. OFF arbors are shown in red. Error bars = standard error of mean. (d-f) Ratio of dendritic and puncta densities of the inner half of the dendritic arbor divided by the outer half. (g) Scatter plot comparing areal density of puncta between ON and OFF arbors of individual cells for all ages recorded. (h) Scatter plots showing the relationship of differences in P/A and D/A between the ON and OFF arbors. ΔP/A = [P/AON - P/AOFF]/[P/AON + P/AOFF]. Similar calculations were obtained for D/A (ΔD/A). R = correlation of coefficient. P-values indicate the probability of producing the given R-value from a random pairing of the data.
Mentions: Our analysis thus far has focused on the synaptic distributions of monostratified cells across development, which is likely to include more than one type of RGC. Bistratified cells, however, provide an opportunity for us to compare the dendritic and synaptic fields of two dendritic arbors within the same cell. To separate the ON and OFF arbors of a bistratified cell, each cell was digitally rotated so that its arbors were orthogonal to the z dimension. We then plotted the distribution of dendritic length along the z dimension and identified the division between ON and OFF arbors by the trough between the two peaks. Dendritic density, areal synaptic density and linear synaptic density are plotted for the ON and OFF arbors of each bistratified cell at various ages in Figure 8. Overall, both the ON and OFF arbors of bistratified cells appeared to follow the same developmental patterns as monostratified cells, although the changes in D/A and P/D were not as pronounced (Figure 8a–f). Bistratified cells, however, exhibited a shallower centro-peripheral gradient compared to monostratified cells: from P7 onwards, the gradient in areal puncta density was significantly lower in the arbors of bistratified cells (1.66 ± 0.10), compared to monostratified cells (1.91 ± 0.08; P = 0.015).

Bottom Line: We found that as dendritic density (dendritic length per unit area of dendritic field) decreases with maturation, the density of synapses along the dendrites increases.The spatial pattern of glutamatergic inputs onto RGCs arises early in synaptogenesis despite ensuing reorganization of dendritic structure.We raise the possibility that these early patterns of synaptic distributions may arise from constraints placed on the number of contacts presynaptic neurons are able to make with the RGCs.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Structure, University of Washington, Seattle, WA 98195, USA. j37@u.washington.edu

ABSTRACT

Background: Neurons receive excitatory synaptic inputs that are distributed across their dendritic arbors at densities and with spatial patterns that influence their output. How specific synaptic distributions are attained during development is not well understood. The distribution of glutamatergic inputs across the dendritic arbors of mammalian retinal ganglion cells (RGCs) has long been correlated to the spatial receptive field profiles of these neurons. Thus, determining how glutamatergic inputs are patterned onto RGC dendritic arbors during development could provide insight into the cellular mechanisms that shape their functional receptive fields.

Results: We transfected developing and mature mouse RGCs with plasmids encoding fluorescent proteins that label their dendrites and glutamatergic postsynaptic sites. We found that as dendritic density (dendritic length per unit area of dendritic field) decreases with maturation, the density of synapses along the dendrites increases. These changes appear coordinated such that RGCs attain the mature average density of postsynaptic sites per unit area (areal density) by the time synaptic function emerges. Furthermore, stereotypic centro-peripheral gradients in the areal density of synapses across the arbor of RGCs are established at an early developmental stage.

Conclusion: The spatial pattern of glutamatergic inputs onto RGCs arises early in synaptogenesis despite ensuing reorganization of dendritic structure. We raise the possibility that these early patterns of synaptic distributions may arise from constraints placed on the number of contacts presynaptic neurons are able to make with the RGCs.

Show MeSH
Related in: MedlinePlus