Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina

Abstract

Three types of light-induced response (L-, RG-, and YRB-type S-potentials) recorded from isolated retinas of the carp (Cyprinus carpio) were identified by their spectral response and later by morphological localization of the recording sites marked with an intracellular Lucifer Yellow (LY). Horizontal cells in a given layer, generating one of the above response types, are electrically coupled via gap junctions, so that the injected LY normally diffused to several neighboring cells. The spatial property of the three types of responses was examined by enlarging the diameter of a light spot (0.25 to 4.0 mm) and displacing the spot (0.5 mm diameter) along a straight 4-mm line which passed over the recording point at the middle. In normal retinas, the half-decay distance of response amplitude with spot displacement was shorter in the order of L-, RG-, and YRB-type responses, and correspondingly the dye diffusion area was narrower in the same order of cells. Dopamine (DA; 10 to 20 PM), applied to the vitreous fluid beneath the isolated retina, altered the spatial property of all types of responses by increasing the amplitude of responses to central spots and decreasing that of those to distant spots, and it restricted the intracellular LY to single injected cells. In contrast, in retinas from which DA interplexiform cells had been deprived by prior destruction with a neurotoxin, 6-hydroxydopamine, the amplitude of responses became smaller while the half-decay distance was longer by l.l-to 1.6-fold, depending upon the cell type, and the dye diffusion area in all types of cells became wider by 2-fold as compared to those in normal retinas. The results indicate that DA regulates the spatial properties of all types of horizontal cells and that there is an apparent correlation between the degrees of S-potential spread (electrical coupling) and of the dye coupling among horizontal cells in a given layer.

Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network

“…This is an additional reason for believing that, although the rod signals are pooled in the cone pedicle at high intensity, they are probably isolated in the rod spherule at low intensity. That the rod-cone gap junctions might be rendered nonconducting during the process of dark adaptation seems plausible in view of evidence that gap junctions between horizontal cells in turtle and fish retina can be modulated by neural transmitters (Lasater and Dowling, 1985;Piccolino et al, 1984;Teranishi et al, 1984) and that rod-rod gap junctions in salamander retina can be voltage-sensitive (Stem and MacLeish, 1985). If, in the present case, the rod-cone gap junctions were modulated, one would want to identify the molecular mechanism, the signal controlling it, and the cell type that conveys the signal.…”

Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network

“…Other retinal gap junctions change their permeability in response to changes in background light intensity, and dopamine mediates many of these effects (Piccolino et al, 1984;Teranishi et al, 1984;McMahon et al, 1989;DeVries & Schwartz, 1989;Hampson et al, 1992;Bloomfield et al, 1997;Mills & Massey, 1995). We undertook this series of experiments in order to determine whether dopamine influenced coupling of OFF α ganglion cells and amacrine cells.…”

Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers.

“…Like other membrane channels, the gap junction channel may be a target for regulation by intracellular messengers. In intact retina, agents that raise the concentration of intracellular cyclic AMP, such as forskolin and isobutylmethylxanthine (IBMX), mimic the effect of dopamine on horizontal cell coupling (Teranishi et al 1983(Teranishi et al , 1984Piccolino et al 1984). By analogy to other more extensively studied systems, dopamine is believed to raise the concentration of cyclic AMP within horizontal cells which in turn may activate a cyclic AMP-dependent protein kinase.…”