BACKGROUND CONTRAST MODULATES KINETICS AND LATERAL SPREAD OF RESPONSES TO SUPERIMPOSED STIMULI IN OUTER RETINA

Surround enhancement (sensitization) is a poorly understood form of ne twork adaptation in which the kinetics of the responses of retinal neu rons to test stimuli become faster, and absolute sensitivity of the re sponses increases with increasing level of steady, surrounding light. Surround enhancement has been observed in all classes of retinal neuro ns in lower vertebrates except cones, in some primate retinal ganglion cells, and in human psychophysical studies. In theory, surround enhan cement could be mediated by two broad classes of mechanisms, which are not mutually exclusive: one in which the kinetics of the transduction linking cone voltage to postsynaptic current in second-order neurons is modulated, and another in which the transformation of postsynaptic current to membrane voltage is modulated. We report here that both cla sses of mechanism play a role in surround enhancement measured in turt le horizontal cells (HCs). We stimulated the retina by modulating sinu soidally the illuminance of a bar placed at various positions in the H C receptive field. The bar was surrounded by either equally luminant o r dim, steady light. Interpretation of responses in the context of a m odel for the cone-HC network led to the conclusion that the speeding u p of response kinetics-due to selective increase in response gain at h igh temporal frequencies-by surround illuminance is almost completely accounted for by the change in the kinetics of the transduction linkin g cone membrane potential to HC postsynaptic current. However, surroun d illuminance also had an additional, surprising effect on the transfo rmation between postsynaptic current and voltage: the space constant f or signal spread in the HC network for the dim-surround condition was roughly twice as large as that for the bright-surround condition. Thus , increasing surround illuminance had analogous effects in the spatial and temporal domains: it restricted the time course and the spatial s pread of signal. Both effects were dependent on the contrast between t he mean bar illuminance and that of the surround, rather than on overa ll light level. When the stimulus with the bright surround was dimmed uniformly by a neutral density filter, the space constant did not incr ease, and response gain at high temporal frequencies did not decrease. Pharmacological experiments performed with dopamine and various agoni sts and antagonists indicated that, although exogenous dopamine can in fluence surround enhancement, endogenous dopamine does not play an imp ortant role in surround enhancement. We conclude that contrast in back ground light modulates the spatiotemporal properties of signal process ing in the outer retina, and does so by a non-dopaminergic mechanism.