Independent influences of rod adaptation on cone-mediated responses to light onset and offset in distal retinal neurons

Abstract

1. The influence of rod adaptation on cone-mediated intracellular responses of distal retinal neurons was examined in the larval tiger salamander. Rods were selectively stimulated by the use of 450-520 nm adapting stimuli too dim to appreciably influence cones. Cones were primarily stimulated with the use of deep-red stimuli (maximally sensitive to wavelengths greater than 650 nm). The qualitative properties of rod-cone interaction were assessed with the use of several different photic-stimulus paradigms. 2. Confirming results of prior studies, we showed that rod adaptation changed the time course of cone-mediated responses to the onset of square-wave light flashes in horizontal cells (HCs); rod adaptation had no similar influence in other distal retinal neurons. Rod adaptation also enhanced cone-mediated responses to rapid flicker in cones, hyperpolarizing (HPBCs) and depolarizing (DPBCs) bipolar cells, as well as HCs. 3. We also examined the influence of rod-stimulating background fields on cone-mediated responses to slow (approximately 1-Hz) flicker composed of sawteeth with a rapid onset (ramp offset) or with a rapid offset (ramp onset). Such stimulation maintained a constant state of long-term adaptation while providing cones with transient-ON or transient-OFF stimulation. 4. Rod adaptation speeds up the response of HCs to rapid onset and increases response amplitude. Rod adaptation had no reliable influence on response to rapid onset in cones or bipolar cells. 5. Rod adaptation enhanced the amplitude of responses of HCs to rapid offset without altering response time course. 6. Rod adaptation greatly enhanced the amplitude of DPBC responses to rapid offset having no reliable influence on the time course of the response. 7. Rod adaptation caused responses of HPBCs to rapid offset to become much more transient. Rod backgrounds had a similar but smaller and less reliable influence on the response of cones to rapid offset. 8. The foregoing results indicate that rod adaptation exerts a minimum of two separate influences on cone-mediated responses in distal amphibian retina. Changes at light onset must reflect the operation of a mechanism that alters response kinetics of the HC membrane. Changes at light offset reflect the operation of a separate mechanism or set of mechanisms that must act in part presynaptically to the HCs.