Centrifugal innervation of the lamprey retina. Light- and electron microscopic and electrophysiological investigations.
Centrifugal fibers and their synaptic connections were studied in retinas of the lamprey Lampetra fluviatilis. The morphological analysis of retinofugal and retinopetal elements was performed after their horseradish peroxidase (HRP) filling through either the cut optic nerve in isolated retina preparations or after intracerebral HRP injections. In flat-mounted retinas, labeled ganglion cell bodies with their dendritic arborizations as well as centrifugal axons were found. The topography of labeled ganglion cell bodies and fibers in semi-thin plastic sections is described. The electron microscopic analysis revealed that the centrifugal terminals synapse either upon unlabeled somata or profiles containing synaptic vesicles (PCSVs). In more rare cases these boutons seem to establish synaptic contacts on ganglion cell dendrites. The target cell bodies were located within the inner part of the inner nuclear layer, whereas postsynaptic dendrites and PCSVs were mainly observed in the outer portion of the internal synaptic layer. Stimulation of the optic nerve in isolated retinas produced antidromic responses in 23 neurons and in 9 of these cells, an antidromic spike was followed by a postsynaptic potential (PSP). Ten cells yielded no antidromic response, but showed PSPs sometimes associated with spikes. The morphological and physiological evidence obtained indicate that these PSP-generating cells were activated synaptically by centrifugal fibers and that in the lamprey retina, these fibers make contacts either with dendrites or somata of amacrine cells and probably with ganglion cell dendrites.