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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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Spatial maps of dendritic and postsynaptic densities of RGCs across development. (a) Dendritic territories are determined by convolving a 10 μm diameter disk centered at every pixel of the image, with the dendritic skeleton (see Materials and methods). Within the dendritic territory of each cell, dendritic length (μm) per 100 μm2 (D/A), puncta per 100 μm2 (P/A), and puncta per micrometer of dendrite (P/D) were obtained. (b) Maps of local values of D/A, P/D, and P/A of OFF monostratified RGCs at different ages. Local densities were determined by counting puncta number and measuring dendritic (Dend) length within a sliding window with a diameter of 20 μm centered at each pixel of the image (see Materials and methods).
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Figure 5: Spatial maps of dendritic and postsynaptic densities of RGCs across development. (a) Dendritic territories are determined by convolving a 10 μm diameter disk centered at every pixel of the image, with the dendritic skeleton (see Materials and methods). Within the dendritic territory of each cell, dendritic length (μm) per 100 μm2 (D/A), puncta per 100 μm2 (P/A), and puncta per micrometer of dendrite (P/D) were obtained. (b) Maps of local values of D/A, P/D, and P/A of OFF monostratified RGCs at different ages. Local densities were determined by counting puncta number and measuring dendritic (Dend) length within a sliding window with a diameter of 20 μm centered at each pixel of the image (see Materials and methods).

Mentions: The dendritic arbors of RGCs can sample from one to hundreds of BC axonal terminals whose mosaic arrangement in the IPL provides a two-dimensional map of visual space [5,24]. We first define the RGC dendritic territory as a two-dimensional area (A) of the retina covered by its dendrites. This territory was obtained by convolving a two-dimensional projection of its dendritic skeleton with a 10 μm diameter disc (average size of a bipolar axon terminal), and then filling in holes in the field (see Materials and methods; Figure 5a, blue region).


Developmental patterning of glutamatergic synapses onto retinal ganglion cells.

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

Spatial maps of dendritic and postsynaptic densities of RGCs across development. (a) Dendritic territories are determined by convolving a 10 μm diameter disk centered at every pixel of the image, with the dendritic skeleton (see Materials and methods). Within the dendritic territory of each cell, dendritic length (μm) per 100 μm2 (D/A), puncta per 100 μm2 (P/A), and puncta per micrometer of dendrite (P/D) were obtained. (b) Maps of local values of D/A, P/D, and P/A of OFF monostratified RGCs at different ages. Local densities were determined by counting puncta number and measuring dendritic (Dend) length within a sliding window with a diameter of 20 μm centered at each pixel of the image (see Materials and methods).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Spatial maps of dendritic and postsynaptic densities of RGCs across development. (a) Dendritic territories are determined by convolving a 10 μm diameter disk centered at every pixel of the image, with the dendritic skeleton (see Materials and methods). Within the dendritic territory of each cell, dendritic length (μm) per 100 μm2 (D/A), puncta per 100 μm2 (P/A), and puncta per micrometer of dendrite (P/D) were obtained. (b) Maps of local values of D/A, P/D, and P/A of OFF monostratified RGCs at different ages. Local densities were determined by counting puncta number and measuring dendritic (Dend) length within a sliding window with a diameter of 20 μm centered at each pixel of the image (see Materials and methods).
Mentions: The dendritic arbors of RGCs can sample from one to hundreds of BC axonal terminals whose mosaic arrangement in the IPL provides a two-dimensional map of visual space [5,24]. We first define the RGC dendritic territory as a two-dimensional area (A) of the retina covered by its dendrites. This territory was obtained by convolving a two-dimensional projection of its dendritic skeleton with a 10 μm diameter disc (average size of a bipolar axon terminal), and then filling in holes in the field (see Materials and methods; Figure 5a, blue region).

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