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Journal of Neuroscience, Vol 12, 1233-1252, Copyright © 1992 by Society for Neuroscience
Bipolar cells specific for blue cones in the macaque retina
N Kouyama and DW Marshak
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77025.
A distinct subpopulation of bipolar cells in macaque monkey retina was
labeled with antisera that recognize glycine-extended cholecystokinin
precursors. The labeled bipolar cells were found throughout the retina and
had dendrites contacting a subpopulation of cone pedicles and axons
ramifying in the fifth stratum of the inner plexiform layer. Several lines
of evidence indicate that the labeled bipolar cells are a single type
despite some variations in their morphology. First, the density of
perikarya and their diameters varied continuously as a function of
eccentricity. Second, the positions of perikarya within the inner nuclear
layer and the level at which the axons branched in the inner plexiform
layer were constant at all eccentricities. Bipolar cells with similar
morphology have been described previously as "blue cone bipolar cells"
(Mariani, 1984b), but there was no direct evidence that this was the case.
In this study, we show by light microscopy that labeled bipolar cells have
dendrites ending exclusively upon presumptive blue cones labeled by Procion
black dye. All blue cones were contacted by labeled bipolar cells, and
virtually all bipolar cells contacted blue cones, the only exceptions being
in regions where blue cones had been lost. Approximately 20% more labeled
bipolar cells than blue cones were found at every eccentricity; thus,
connections between blue cones and labeled bipolar cells were not strictly
one to one. The mean number of cones presynaptic to each bipolar cell was
1.2, and the mean number of bipolar cells postsynaptic to each cone was
1.8. By an electron microscopic study of labeled bipolar cell dendrites, we
determined that they became central elements of ribbon synapses in blue
cones. Some of their ribbon synapses were unusual: in one type, a single,
large labeled dendrite was postsynaptic to two or more ribbons, while in
the other type, ribbons had two or more central elements. The presence of
these invaginating contacts and the axonal terminals in the proximal inner
plexiform layer suggest that the labeled bipolar cells depolarize to
short-wavelength stimuli and function to relay information from blue cones
to the inner plexiform layer. There were also other, unlabeled bipolar cell
dendrites that received inputs from blue cones at basal junctions and
triad-associated flat contacts, which suggests that there are additional
types of bipolar cells conveying information from short- wavelength cones
in the primate retina.
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