Receptive field organization of ganglion cells in the frog retina: contributions from cones, green rods and red rods

Abstract

1. The impulse discharge of ganglion cells was recorded with extracellular micro-electrodes in the excised and opened eye of the common frog, Rana temporaria. 2. When a single unit was isolated, the cell type was first determined according to the Maturana, Lettvin, McCulloch & Pitts (1960) classification with the aid of varying moving and stationary stimuli. 3. Class 4 cells respond only to a decrease of light when cones are stimulated but respond to an increase of light when green rods are stimulated. A distinct class of deviating class 4 cells was found that give a brief high frequency burst at 'off' from their small excitatory receptive fields (ERF); unlike typical class 4 cells they possess a purely inhibitory surrounding field (IRF).4. The contributions from the cones and the green and red rods were isolated by measuring the thresholds of the discharges with on-off stimuli of varying wave-lengths against strong yellow backgrounds, or against a very weak background or no background at all. The spatial distribution of the contributions to the ERF was determined by mapping threshold profiles, and additional information about ERF and IRF was obtained from area-threshold curves. 5. The cone-mediated ERFs were found to be 0-06-0-50 mm wide (1-5-12 degrees of visual field), which agrees well with the sizes of the dendritic trees of the ganglion cells. The green rod-mediated ERFs can be 0-5-1-5 mm wide and have less distinct boundaries than the cone-mediated. The green rod-mediated ERF of an individual ganglion cell is always larger than the cone-mediated ERF of the same cell. The red rod-mediated ERFs seem to be somewhat larger than the cone-mediated but smaller than the green rod-mediated. 6. The green rods contribute only to the on thresholds of class 1, 2 and 4 cells, but both to on and off in typical class 3 cells, while the cones contribute to on and off in classes 1-3 and only to off in class 4.7. When the red rods begin to contribute during dark adaptation they seem to enter the cone but not the green rod channels. 8. All three receptor types contribute to the IRF surrounding the ERF of classes 1, 2, 3 and deviating class 4 cells. Normal class 4 cells have no IRF. 9. The organization of the receptive fields is discussed in relation to the anatomy and electrophysiology of the cell types transmitting the signals from the receptors to the ganglion cells.