MODULATION OF SUSTAINED AND TRANSIENT LATERAL INHIBITORY MECHANISMS IN THE MUDPUPPY RETINA DURING LIGHT ADAPTATION

Two functionally and anatomically distinct types of lateral inhibition contribute to the receptive field organization of ganglion cells in t he vertebrate retina: sustained lateral inhibition (SLI), which is pre sent during steady illumination and transient lateral inhibition (TLI) , evoked by changes in illumination. We studied adaptive changes in th ese two lateral inhibitory mechanisms in the mud-puppy puppy retina by measuring the responses of ON-OFF ganglion cells to spots of light in the receptive field center, in the absence and presence of a concentr ic broken annulus (windmill) pattern, which was either stationary or r otating. SLI was measured as the percent suppression of the centered s pot response by the stationary windmill and TLI was measured as the ad ditional suppression produced when the windmill was rotating. In dark- adapted retinas SLI was elicited by windmills of 600 or 1,200 mu m ID, but TLI could not be elicited by windmills of any size, over a wide r ange of windmill intensities and rotation rates. Exposure of dark-adap ted retinas to diffuse adapting light caused an immediate decrease in the response to the spot alone, followed by slowly developing changes in both SLI and TLI: SLI produced by 1,200 mu m ID windmills became we aker, whereas SLI produced by 600 mu m ID windmills became stronger. A fter several minutes strong TLI could be elicited by both 600 and 1,20 0 mu m ID windmills. The changes in SLI and TLI were usually complete within 5 and 15 min, respectively, and recovered to dark-adapted level s slightly more slowly after the adapting light was turned off. Howeve r the changes in sensitivity of the spot response were complete within one minute after onset and termination of the adapting light. The ada ptive changes in SLI and TLI did not depend on the presence of the ada pting light; after a brief (1 min) exposure to the adapting light, the changes in SLI and TLI slowly developed and then decayed back to the dark-adapted level. The effects of the adapting light on SLI were mimi cked by dopamine and blocked by D1 dopamine receptor antagonists. Howe ver dopamine did not enable TLI in dark-adapted retinas and dopamine a ntagonists did not prevent enablement of TLI when dark-adapted retinas were exposed to light or disable TLI when applied to light-adapted re tinas. The results suggest that light-adaptive changes in SLI are medi ated by dopamine and are consistent with a reduction in electrical cou pling between neurons that conduct the SLI signal laterally in the ret ina. In contrast, TLI appears to be switched off or suppressed in the dark-adapted retina and enabled in light-adapted retinas, by a relativ ely slow modulatory mechanism that does not involve dopamine.