Abstract
Purpose: :
Human and macaque monkey retinae contain ∼3000 melanopsin–expressing, inherently photosensitive ganglion cells. These cells have the largest dendritic trees of any primate ganglion cell type and have therefore been called giant cells. The giant cells are also strongly driven by rod and cone pathway input (Dacey, Nature 433:749, 2005). Giant cells can be divided into two groups stratified either at the extreme outer or inner border of the inner plexiform layer (IPL). Here we further characterize the morphology of the inner and outer giant cells and show that they make contact respectively with the DB6 cone bipolar cell type (inner border of the IPL) and with the dopaminergic amacrine cell (outer border of the IPL).
Methods: :
Rabbit polyclonal antibodies derived from c–DNA for human melanopsin were used to immunolabel fixed human and macaque retina. Sheep anti–tyrosine hydroxylase and mouse anti–CD15 were used for double–labeling with the melanopsin antibody; confocal microscopy was used to analyze relative stratification and loci of putative synaptic contact.
Results: :
In macaque, inner stratifying melanopsin immunoreactive cells have larger dendritic fields and cell bodies and more highly branched dendritic trees than outer cells; human counterparts show similar disparities. Inner and outer giant cell bodies form independent, regularly arranged spatial arrays (nearest neighbor analysis: regularity index: 2.6, inner cells, 2.9, outer cells). Outer giant cell dendrites costratify with and appear to extensively contact the fine, axon–like processes of the dopaminergic amacrine cells; the dopaminergic processes follow and closely appose all parts of the giant cell tree and soma, dramatically enmeshing and 'outlining' the complete morphology of the ganglion cell. CD15 stained DB6 bipolar cell axons stratify against the outer margin of the inner giant cell processes; spines arising from the DB6 axons often descend to come into apposition with distinct spines on the giant cell dendrites. For one double–labeled giant cell, total putative DB6 contacts was ∼169, spread regularly over the entire dendritic tree, comprising ∼7% of total dendritic length.
Conclusions: :
In primates, the melanopsin–containing giant cells form two anatomically independent populations. Outer cells make extensive and intimate contact with the dopaminergic plexus; inner cells appear to receive a specific input from the DB6 cone bipolar type.
Keywords: ganglion cells • retina: proximal (bipolar, amacrine, and ganglion cells) • retinal connections, networks, circuitry