Physiological and morphological properties of OFF- and ON-center bipolar cells in the Xenopus retina: Effects of glycine and GABA

Abstract

We studied the morphology and center-surround organization of Lucifer Yellow injected OFF- and ON-center bipolar cells in the light-adapted Xenopus retina and the effects of glycine and GABA on their cone-mediated light responses. In both classes of cell, prominent antagonistic surround responses up to 20 mV in amplitude could be evoked without first suppressing the center responses with steady illumination. An additional feature of the light-evoked bipolar cell response was a pronounced (up to –24 mV) delayed hyperpolarizing after potential (DHAP) which followed the depolarizing responses of both classes of bipolar cell.The morphological features of dye-injected bipolar cells conformed to the general idea of segregation of ON and OFF pathways in the inner and outer interplexiform layer, however, the morphology of axonal arborizations was different for both classes. OFF-center cells ramified symmetrically around the primary branchpoint, whereas ON-center cells had a strongly asymmetrical arrangement of their axonal tree.The center and surround responses were differentially sensitive to glycine and GABA. Glycine eliminated the antagonistic surround responses in both OFF and ON cells; the center responses were reduced to some extent but were not eliminated. In contrast, GABA affected the hyperpolarizing responses much more strongly than the depolarizing response components. That is, the amplitude of the center response in the OFF cell and the surround response in the ON cell was reduced 80–90% during exposure to GABA, whereas the surround and center depolarizations of OFF and ON cells, respectively, were reduced only 0–10%.Our findings implicate a role for GABAergic and glycinergic pathways in the center-surround organization of bipolar cells in Xenopus retina. In addition, the results suggest that the pathways mediating center-surround antagonism may be different in OFF-bipolar cells vs. ON-bipolar cells.

Immunocytochemical study of glycine receptors in the retina of the frog Xenopus laevis

“…The comparison between the puncta enclosed shows that co-localizations between them exist. Scale bar 20 lm ment with the electrophysiological data according to which glycine is involved in the surround responses of both on-and off-bipolar cells in X. laevis retina (Stone and Schu¨tte 1991). Our results are in agreement with the immunocytochemical data of other authors who have also demonstrated glycine receptors in the lower verte- Fig.…”

“…A question of interest arose: if the GlyRs in these two kindred types of amphibian retinae differ or not. The results presented here give answer to this question allowing comparison of the GlyRs in the retina of X. laevis with those in the retina of R. ridibunda, two species widely used in electrophysiological experiments (Stone and Schu¨tte 1991;Popova et al 1997Popova et al , 2000.…”

Synaptology of the inner plexiform layer in the anuran retina

“…At the same time, however, GABA in the ON pathway may more efficiently control receptive field, center-surround, and spatial frequency mechanisms than in the OFF pathway in anurans (Bonaventure and Wioland, 1981). This is in agreement with the results of physiological studies that found differential sensitivity of ON and OFF circuitries to GABA and glycine (Bonaventure et al, 1980;Stone and Schü tte 1991).…”

Effects of picrotoxin on light adapted frog electroretinogram are not due entirely to its action in proximal retina

“…Most of the studies were performed by using one or narrow range of stimulus intensities and the results obtained are contradictory. While some authors reported that GABA diminishes and GABA antagonists (bicuculline, picrotoxin) enhance the light responses of ON bipolar cells (mudpuppy: Miller, Slaughter, & Dick, 1982;Miller et al, 1981), other authors have not obtained any effect of GABA on them (xenopus: Stone & Shutte, 1991). Still other authors suggest that the effect of GABA on the amphibian ON bipolar cells may be related only to the time characteristics of the light responses and not to their amplitude.…”

“…Inconsistent results have been obtained also for the GABA effects on the amphibian OFF bipolar cells. Some authors reported that antagonists of ionotropic GABA receptors have no effect on their light responses (mudpuppy: Daniels, 1974;Miller et al, 1981), while other authors reported their suppression under the influence of GABA (Hare & Owen, 1996;Stone & Shutte, 1991) or GABA antagonists picrotoxin and bicuculline (Hare & Owen, 1996). Our results indicate that GABA, released in both the outer and inner plexiform layer in frog retina, acts to diminish the amplitude and speed up the time course of the cone-mediated light responses of both ON and OFF bipolar cells.…”