We studied feedback from horizontal cells to cones in isolated goldfish retinae and found that surround stimuli evoke an inward current and a slowly developing outward current. The surround-evoked currents are blocked by the glutamate antagonist 6,7-dinitroquinoxaline-2,3-dione (DNQX) and are, like horizontal cell responses, most effectively evoked by large stimuli. This indicates that the currents are caused by feedback from horizontal cells. The surround-evoked inward current is neither blocked by picrotoxin nor carried by chloride. Instead, it is carried by calcium, and it triggers a slowly developing calcium-dependent chloride current. We were unable to mimick the surround-evoked currents by modulating the extracellular GABA concentration. We conclude that when horizontal cells hyperpolarize they feed back to the cones by shifting the cone calcium-current activation range to more negative potentials. This type of feedback, directly targeted at the calcium current, scarcely influences the membrane potential of the receiving neuron, but effectively modulates its synaptic output.

Center-surround antagonism is a hallmark feature of the receptive fields of sensory neurons. In retinas of lower vertebrates, surround antagonism derives in part from inhibition of cone photoreceptors by horizontal cells. Using whole-cell patch recording methods, we found that light-evoked responses of cones in macaque monkey were antagonized when surrounding cones were illuminated. The spatial and spectral properties of this antagonism indicate that it results from inhibition by horizontal cells. It has been suggested that horizontal cell inhibition is mediated by the neurotransmitter GABA. The inhibition observed here, however, was inconsistent with a GABA-gated chloride conductance mechanism. Instead, surround illumination evoked an increase in calcium conductance and calcium-activated chloride conductance in cones. We expect that these conductances modulate neurotransmitter release at the cone synapse and increase visual sensitivity to spatial contrast.

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