Functional morphology of frog retinal ganglion cells and their central projections: the dimming detectors

Intracellular recordings were made from frog retinal ganglion cell axons in the optic nerve. Following electrophysiological characterisation of receptive field properties, HRP was injected into the axon, and the brain and retina were subsequently stained. The morphologies of retinal ganglion cells, their dendritic domains, and their central projections were determined with light microscopy, and the optic nerve portion of the ganglion cell axon was examined with electron microscopy. This paper describes the structural and functional features of one ganglion cell class, the off units (class IV or dimming detectors) whose characteristic response is a preferential sensitivity to decreasing light intensity within the receptive field. Typical receptive field diameter of these units was about 16 degrees with a range of 3 degrees to more than 30 degrees. Examination of the spatial characteristics of their receptive field centers and surrounds showed that the class IV cells could be divided into two broad categories. Linear class IV cells did not respond to phase-reversal of a fine grating pattern. These linear cells also tended to have clear surround suppression: illumination of the surround diminished their response to light off at the center. The second group responded briskly to each reversal of the fine grating pattern, whatever its position within the receptor field center. These nonlinear class IV cells did not show surround suppression, but rather they had surround antagonism and they responded to light on in the surround. Nonlinear units were much more frequently recorded in frogs maintained in summer conditions (12-hour days, constant 20 degrees C temperature). In spite of this functional heterogeneity, all cells had similar morphology consisting of a large ganglion cell with a large dendritic arbor (400-1,000 microns) confined to a single stratum in the outer third of the inner plexiform layer, a medium-sized axon (2.4-microns diameter), a smallish pretectal arbor, and a large tectal arbor (300-700 microns) at layer 8.