Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit

Abstract

Retinal ganglion cells are the projection neurons that link the retina to the brain. Peptide immunoreactive cells in the ganglion cell layer (GCL) of the mammalian retina have been noted but their identity has not been determined. We now report that, in the rabbit, 25-35% of all retinal ganglion cells contain substance P-like (SP) immunoreactivity. They were identified by either retrograde transport of fluorescent tracers injected into the superior colliculus, or by retrograde degeneration after optic nerve section. SP immunoreactive cells are present in all parts of the retina and have medium to large cell bodies with dendrites that ramify extensively in the proximal inner plexiform layer. Their axons terminate in the dorsal lateral geniculate nucleus, superior colliculus and accessory optic nuclei, and these terminals disappear completely after contralateral optic nerve section and/or eye enucleation. In the dorsal lateral geniculate nucleus large, beaded, immunoreactive axons and varicosities make up a narrow plexus just below the optic tract, where they define a new geniculate lamina. The varicosities make multiple synaptic contacts with dendrites of dorsal lateral geniculate nucleus projection neurons and presumptive interneurons in complex glomerular neuropil. This is direct evidence that some mammalian retinal ganglion cells contain substance P-like peptides and strongly suggests that, in the rabbit, substance P (or related tachykinins) may be a transmitter or modulator in a specific population or populations of retinal ganglion cells.

Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity.

“…Both of these methods, however, are subject to error, since it is difficult to determine that all ganglion cells degenerate after axotomy or transport HRP retrogradely. Our analysis of the GCL of the rabbit retina employed both of these experimental approaches (32,33). The distribution and density of neurons in the GCL after optic nerve transection and extended survival periods (32) are in close agreement with the pattern and density of neurons that did not contain HRP reaction product after multiple injections of this enzyme into the superior colliculus (33).…”

“…A smaller number of lightly stained medium-to large-size cell bodies, encountered most frequently in central retinal regions, were also observed. In retinas whose optic nerve was transected, and after a survival period sufficiently long to eliminate most ganglion cells (9,32), there was no change in the number of small GABA-ir cells in the GCL, but there was a substantial reduction in the number of mediumto large-size GABA-ir cells. These observations suggest that (Table 1).…”

“…Our analysis of the GCL of the rabbit retina employed both of these experimental approaches (32,33). The distribution and density of neurons in the GCL after optic nerve transection and extended survival periods (32) are in close agreement with the pattern and density of neurons that did not contain HRP reaction product after multiple injections of this enzyme into the superior colliculus (33). The HRP retrograde-transport study also provides a basis for dividing nonlabeled neurons into two general groups, one having a small somal size, which was counted for Fig.…”

Neurotransmitters, receptors, and neuropeptides in the accessory optic system: An immunohistochemical survey in the pigeon (Columba livia)

“…However, we did not observe NT-labeled ganglion cells projecting to the pigeon nBOR in a recent study (Britto etal., 1988). Substance P has been shown to occur in the retinal projection to the rabbit AOS (Brecha et al, 1987) and in the retinal projection to the tectal system in both anurans (Kuljis & Karten, 1983 and chickens (Ehrlich et al, 1987). The presence of SP-positive fibers has been reported in the AOS in a mapping study of the turtle brain, although the SP-positive fibers were restricted to a region that appears equivalent only to the avian nBORd (Reiner et al, 1984).…”

“…There appear to be only three reports on putative transmitters in the ganglion cells projecting to the AOS. The first indicates the occurrence of substance P-like immunoreactivity in such cells in the rabbit (Brecha et al, 1987). The second demonstrated that approximately 10% of the displaced retinal ganglion cells projecting upon the pigeon accessory optic nucleus exhibit tyrosine hydroxylase-like immunoreactivity .…”