Horizontal cells feed back to cones by shifting the cone calcium-current activation range

Abstract

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.

Hydrogen Sulfide Protects the Retina from Light-induced Degeneration by the Modulation of Ca2+ Influx

“…The negative feedback from horizontal cells to photoreceptor cells plays an important role in the center-surround organization (30). Feedback from horizontal cells to photoreceptor cells is mediated by the suppression of L-type Ca 2ϩ channels on photoreceptor cells by protons released from V-ATPase on horizontal cells (31)(32)(33)(34). V-ATPase has two cysteine residues at the ATP-binding site of catalytic subunit and reversible formation of disulfide bond results in inactivation of the V-ATPase (35).…”

“…The proposed mechanisms for the feedback are the changes in pH in the synaptic cleft and the involvement of GABAergic neurons (31)(32)(33)(34)38). The present study shows that H 2 S activates V-ATPase to suppress high K ϩ evoked Ca 2ϩ influx mediated by L-type Ca 2ϩ channels (Fig.…”

Synaptic transmission at retinal ribbon synapses

“…Kamermans and his co-workers (Verweij et al, 1996;Kraaij et al, 2000;Kamermans et al, 2001; reviewed in Kamermans and Fahrenfort, 2004) have elaborated a hypothesis whereby feedback shifts the operating range of the I Ca in cones. In the goldfish retina, illuminating the cone with a surround displaced the Ca-activation curve to the left by about −7.5 mV.…”

c-Fos expression in the visual system of the tree shrew (Tupaia belangeri)

“…Lateral inhibitory interactions in the OPL contribute to the surround portion of the receptive fields of bipolar and ganglion cells (Werblin and Dowling, 1969;Mangel, 1991;McMahon et al, 2004). However, several studies suggest that the OPL generated surround signal is not mediated by GABA (Verweij et al, 1996;Kamermans et al, 2001;Verweij et al, 2003;McMahon et al, 2004). In contrast, lateral inhibition in the IPL, which contributes to the surround of ganglion cells, is mediated by GABA (Cook and McReynolds, 1998;Flores-Herr et al, 2001).…”