Spatial distribution of excitatory synapses on the dendrites of ganglion cells in the mouse retina

PLoS One. 2014 Jan 17;9(1):e86159. doi: 10.1371/journal.pone.0086159. eCollection 2014.

Abstract

Excitatory glutamatergic inputs from bipolar cells affect the physiological properties of ganglion cells in the mammalian retina. The spatial distribution of these excitatory synapses on the dendrites of retinal ganglion cells thus may shape their distinct functions. To visualize the spatial pattern of excitatory glutamatergic input into the ganglion cells in the mouse retina, particle-mediated gene transfer of plasmids expressing postsynaptic density 95-green fluorescent fusion protein (PSD95-GFP) was used to label the excitatory synapses. Despite wide variation in the size and morphology of the retinal ganglion cells, the expression of PSD95 puncta was found to follow two general rules. Firstly, the PSD95 puncta are regularly spaced, at 1-2 µm intervals, along the dendrites, whereby the presence of an excitatory synapse creates an exclusion zone that rules out the presence of other glutamatergic synaptic inputs. Secondly, the spatial distribution of PSD95 puncta on the dendrites of diverse retinal ganglion cells are similar in that the number of excitatory synapses appears to be less on primary dendrites and to increase to a plateau on higher branch order dendrites. These observations suggest that synaptogenesis is spatially regulated along the dendritic segments and that the number of synaptic contacts is relatively constant beyond the primary dendrites. Interestingly, we also found that the linear puncta density is slightly higher in large cells than in small cells. This may suggest that retinal ganglion cells with a large dendritic field tend to show an increased connectivity of excitatory synapses that makes up for their reduced dendrite density. Mapping the spatial distribution pattern of the excitatory synapses on retinal ganglion cells thus provides explicit structural information that is essential for our understanding of how excitatory glutamatergic inputs shape neuronal responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Size
  • Dendrites / metabolism*
  • Disks Large Homolog 4 Protein
  • Female
  • Green Fluorescent Proteins / metabolism
  • Guanylate Kinases / metabolism
  • Male
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Recombinant Fusion Proteins / metabolism
  • Retinal Ganglion Cells / cytology
  • Retinal Ganglion Cells / metabolism*
  • Synapses / metabolism*

Substances

  • Disks Large Homolog 4 Protein
  • Dlg4 protein, mouse
  • Membrane Proteins
  • Recombinant Fusion Proteins
  • Green Fluorescent Proteins
  • Guanylate Kinases

Grants and funding

This study was supported by the National Science Council of Taiwan NSC-98-2311-B-007-004-MY3 and NSC-101-2628-B-007-001-MY3 (to CCC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.