Structural and functional properties of two types of horizontal cell in the skate retina.

Abstract

Two morphologically distinct types of horizontal cell have been identified in the all-rod skate retina by light-and electron-microscopy as well as after isolation by enzymatic dissociation. The external horizontal cell is more distally positioned in the retina and has a much larger cell body than does the internal horizontal cell. However, both external and internal horizontal cells extend processes to the photoreceptor terminals where they end as lateral elements adjacent to the synaptic ribbons within the terminal invaginations.Whole-ceU voltage-clamp studies on isolated cells similar in appearance to those seen in situ showed that both types displayed five separate voltage-sensitive conductances: a TTX-sensitive sodium conductance, a calcium current, and three potassium-mediated conductances (an anomalous rectifier, a transient outward current resembling an A current, and a delayed rectifier). There was, however, a striking difference between external and internal horizontal cells in the magnitude of the current carried by the anomalous rectifier. Even after compensating for differences in the surface areas of the two cell types, the sustained inward current elicited by hyperpolarizing voltage steps was a significantly greater component of the current profile of external horizontal cells. A difference between external and internal horizontal cells was seen also in the magnitudes of their TEA-sensitive currents; larger currents were usually obtained in recordings from internal horizontal cells. However, the currents through these K § channels were quite small, the TEA block was often judged to be incomplete, and except for depolarizing potentials >__ + 20 mV (i.e., outside the normal operating range of horizontal cells), this current did not provide a reliable indicator of cell type.The fact that two classes of horizontal cell can be distinguished by their electrophysiological responses, as well as by their morphological appearance and spatial distribution in the retina, suggests that they may play different roles in the processing of visual information within the retina.

Cellular localization of the vesicular inhibitory amino acid transporter in the mouse and human retina

“…GABA release in horizontal cells is generally thought to occur by a transporter-mediated mechanism. This unconventional GABA release was first described in the amphibian and fish retina (Schwartz, 1982(Schwartz, , 1987Yazulla andKleinschmidt, 1982, 1983;Ayoub et al, 1984) where GABA transporters are expressed in horizontal cells and generate measurable currents (Malchow et al, 1990;Cammack and Schwartz, 1993;Dong et al, 1994). In agreement with this hypothesis, classic synaptic specializations were not observed in horizontal cell processes (Yazulla, 1995), except for human horizontal cells (Linberg and Fisher, 1988).…”

Potassium Currents Distinguish the Two Subtypes of Morphologically Distinct Skate Bipolar Cells

“…4B). The currents activate rapidly at depolarizing voltages Ն Ϫ20 mV, they deactivate quickly after membrane repolarization, and the I-V relation appears to have a profile similar to that of the delayed rectifier (e.g., the Kv3 channel family) observed in many other preparations (5,6).…”

pH Regulation in Horizontal Cells of the Skate Retina

“…The procedure for obtaining isolated horizontal cells has been described in detail previously (Malchow et al, 1990). Briefly, eyes were enucleated from skate (Raja erinacea and Raja ocellata) that had been sedated on ice, and pithed both anteriorly and posteriorly.…”

“…Only the large external horizontal cells of the skate retina, viewed under phase contrast optics and readily identified by their characteristic morphology (Malchow et al, 1990), were used for this study. For voltage-clamp experiments, membrane currents were monitored using the whole-cell version of the patchclamp technique (Hamill et al, 1981), and details of the recording were reported previously (HaughScheidt, Malchow and Ripps, 1995).…”

“…As in all other vertebrate species studied thus far, skate horizontal cells receive direct synaptic input from the photoreceptors, they are depolarized by glutamate and other excitatory amino acids (Dowling and Ripps, 1973 ;Lasater, Dowling and Ripps, 1984), they are strongly coupled via pHsensitive gap junctions (Qian and Ripps, 1992 ;Qian, Malchow and Ripps, 1993), and they display a large complement of voltage-gated membrane channels (Malchow et al, 1990). The approach we have taken is to examine the recovery of pH i from an experimentally-imposed acid load, a fundamental technique that has been successfully applied to the study of pH i regulation in a broad range of tissues (cf.…”