Depolarization elicits, while hyperpolarization blocks uptake of endogenous glutamate by retinal horizontal cells of the turtle

Abstract

We have employed an immunoreaction against glutamate to qualitatively demonstrate varying levels of glutamate in retinal horizontal cells of the turtle. Glutamate-like immunoreactivity (GLI) in horizontal cells could be demonstrated after glutamate decarboxylase was inhibited by aminooxyacetic acid (AOAA) and its degradation to GABA was blocked. Depolarization of horizontal cells by kainic acid (KA) induces strong glutamate immunoreactivity in these cells, whereas hyperpolarization by 2,3-cis piperidine dicarboxylate (PDA) abolishes glutamate-like immunoreactivity in horizontal cells. When glutamate release from cones and bipolar cells is blocked in the absence of calcium, or when glutamate uptake is blocked by DL-threo beta-hydroxy aspartate, KA/AOAA treatment of the retina does not induce GLI in horizontal cells. Our data show that horizontal cells are capable of taking up glutamate from the endogenous retinal pool in an activity dependent way. Our interpretation of these findings is that retinal horizontal cells are capable of regulating glutamate levels in the extracellular space of the cone pedicle complex by an activity-dependent uptake system. We suggest that inhibition of glutamate uptake upon hyperpolarization rather than inhibition of GABA release may evoke the antagonistic surround response of retinal bipolar cells.

Sign‐preserving and sign‐inverting synaptic interactions between rod and cone photoreceptors in the dark‐adapted retina

“…6), suggesting that glutamate transporter‐mediated chloride channels are involved in the HC→cone feedback synapse, but not in the rod→HC synapse. A requirement of such glutamate transporter‐mediated HC→cone feedback synapse is that HCs must release glutamate under certain conditions, and a previous study from fish HCs suggest just that (Schutte & Schlemermeyer, 1993). An alternative (but not mutually exclusive) explanation of the TBOA result is that glutamate transporter‐mediated chloride channels are involved in the direct rod→cone, sign‐inverting chemical synapse (Lasansky, 1973).…”

“…Among synaptic blockers/modulators that have been implicated to block the HC→cone feedback synapses, we found that TBOA suppresses I RC without affecting I HC , suggesting that glutamate transporter‐mediated chloride channels are involved in the HC→cone feedback synapse, but not in the rod→HC synapse. A requirement of such glutamate transporter‐mediated HC→cone feedback synapse is that HCs must release glutamate under certain conditions, and a previous study from fish HCs suggests just that (Schutte & Schlemermeyer, 1993).…”

Differential expression of three glutamate transporter subtypes in the rat retina

“…If true, such an activity-dependent glutamate uptake could antagonize bipolar cell light responses. However, in artificial expression systems (Kanai et al 1994), EAAC-1 has been shown to have electrogenic characteristics which are exactly the opposite to those postulated by Schütte and Schlemermeyer (1993). Upon depolarization, glutamate uptake is reduced and during hyperpolarization uptake of glutamate by EAAC-1 is increased.…”

“…Müller cell processes, as mentioned above, are not inserted into the photoreceptor ribbon synapses, hence uptake of glutamate may also have to be performed by photoreceptors, horizontal cells or bipolar cells. Schütte and Schlemermeyer (1993) have recently demonstrated that horizontal cells of the turtle retina exhibit an activity-dependent uptake of glutamate: depolarization elicits, while hyperpolarization blocks uptake of endogenous glutamate. This raises the possibility that horizontal cells are capable of regulating glutamate levels in the extracellular space of the synaptic complex in cone pedicles and rod spherules.…”

“…This raises the possibility that horizontal cells are capable of regulating glutamate levels in the extracellular space of the synaptic complex in cone pedicles and rod spherules. Horizontal cells are hyperpolarized upon illumination and Schütte and Schlemermeyer (1993) proposed that this causes a reduction in their glutamate uptake -more glutamate is left in the synaptic terminal of photoreceptors, which then signals "less light" to the bipolar cells. If true, such an activity-dependent glutamate uptake could antagonize bipolar cell light responses.…”