The proximal negative response and visual adaptation in the skate retina.

Abstract

A B S T R A C T The proximal negative response (PNR), a complex extracellular potential derived mainly from amacrine cell activity, was studied in the all-rod retina of the skate. Tetrodotoxin (10 -6 mg/ml) did not affect either the waveform or the latency of the response, indicating that the PNR reflects the graded, nonregenerative components of the amacrine cell potential. As regards its adaptive properties, the PNR exhibited both the extreme sensitivity to weak background light and the slow time course of light and dark adaptation that are characteristic of other responses from the proximal retina. Thus, the PNR, like the b-wave and ganglion cell discharge, appears to reflect adaptive processes located within the neural network of the inner retina. I N T R O D U C T I O NIn previous studies we described the adaptive properties of retinal potentials arising f r o m different levels within the all-rod retina of the skate (Dowling and Ripps, 1970, 1971, 1972Green et al., 1975). O u r results suggest that there are two principal stages at which visual thresholds are regulated during light and dark adaptation. One adaptive mechanism is located within the photoreceptors and affects equally the sensitivities of the receptors and the horizontal cells, the other (the "network" mechanism) is located more proximally and exerts its effect on the thresholds for both the b-wave and ganglion cell responses. However, neither the cellular nor the ionic basis of network adaptation has been identified as yet (but cf. Dowling and Ripps, 1976).In an a t t e m p t to f u r t h e r this analysis, we have e x a m i n e d the adaptive characteristics of the proximal negative response (PNR) of the skate retina. Several lines of evidence suggest that this complex retinal potential is mainly the extracellular expression of amacrine cell activity (Burkhardt, 1970; Proenza and B u r k h a r d t , 1973). Because the amacrine cells are in synaptic contact with bipolar and ganglion cells, as well as with other amacrine cells (Dowling and Boycott, 1966), it is i m p o r t a n t to establish the role of these i n t e r n e u r o n s in visual adaptation. We find that the behavior of the PNR during light and dark adaptation resembles in m a n y respects that of the b-wave and ganglion cell discharge. And although there are some small differences a m o n g the adaptive properties of these different responses, we conclude that PNR thresholds, like those of other responses of the proximal retina, are affected by the processes governing network adaptation.

A rise in intracellular Ca2+ underlies light adaptation in dogfish retinal ‘on’ bipolar cells

“…This is paralleled by a 3000-fold elevation in human visual threshold following light adaptation of the rod system, whilst at the same time the reduction in gain in phototransduction is only some 5_fold (Thomas & Lamb, 1998). The b-wave of the electroretinogram (ERG), which derives from the population of 'on' bipolar cell responses (Falk & Shiells, 1995), displays the same shift of adaptive characteristics as 'on' ganglion cells (Dowling & Ripps, 1977) and human subjective visual changes. These observations have given rise to the concept of adaptation of the rod pool (Rushton, 1965) or network adaptation due to the release of some 'desensitizing substance', possibly K¤, accumulating in the inner layer of the retina (Dowling & Ripps, 1977).…”

On the duplex nature of the skate retina

“…Voltage-intensity data obtained in the presence of the dim background field were shifted about 1 logarithmic unit to the right on the intensity axis, and the maximum response that could be elicited was greatly reduced. Skate ganglion cells also show decreased sensitivity when the retina is illuminated with such dim light, and the loss of incremental sensitivity is the same as seen for the PNR and b-wave potentials Dowling and Ripps, 1977). Considering that the receptoral and horizontal-cell responses are unaffected by this level of ambient illumination, it is likely that the adaptive changes occurring in the proximal retina are governed by postreceptoral mechanisms.…”

Convergence and Segregation of the Multiple Rod Pathways in Mammalian Retina

“…Response thresholds for individual cells were taken as 5% of maximal spike frequency. Changes in the adaptational state of the retina will result in changes in the sensitivities of individual cells, resulting in a shift in their intensityresponse functions along the abscissa (Green et al, 1975;Dowling and Ripps, 1977). So that the intensity-response functions of different cells in different retinas could be compared, it was thus imperative to maintain all cells in this study under the same adaptational conditions.…”