Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina

Abstract

SUMMARY1. Intracellular recordings of cone and horizontal cell responses to circles or annuli of light were made with the purpose of determining the properties of and the mechanisms underlying the horizontal-cell-mediated depolarization of cones which is evoked by surround illumination.2. A comparison of the responses of a cone and a near-by horizontal cell to a peripheral stimulus revealed a striking similarity in their time courses and amplitudes, indicating that a correlation exists between the depolarizing synaptic potential in the cone and the response of the horizontal cell.3. The depolarizing synaptic potential in cones was separated from the direct response of the cell to light by illuminating the periphery with an annulus during steady, bright illumination of the central cone. The synaptic potentials were graded with the intensity or area of peripheral illumination. In some cones a spike-like depolarization, which overshot the dark resting potential, occurred with bright illumination of the periphery.4. The effects of extrinsic current on the synaptic potential demonstrated that this response was generated by a change in membrane conductance consisting of two separate components with different timedependences and reversal levels. The slower of the two components, which often outlasts the stimulus, represents an increase in membrane conductance.5. The progressive decline in the amplitude of the responses of horizontal cells under a large spot from centre to periphery was found to result in a diminished feed-back effect in cones near the edge of the spot. This leads to a Mach-band effect during the plateau phase of cone responses, * Present address: Physiological Laboratory, Cambridge CB2 3EG, England. P. M. O'BRYAN suggesting that one function of the feed-back might be to enhance contrast discrimination.

Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive field surround.

“…11). (b) Spikes illustrated in previous reports (O'Bryan, 1973;Fuortes et al 1973; were found in the absence of a prolonged depolarization. (c) In the vast majority of cones in our sample in which the prolonged depolarization was well developed, spikes were not evident.…”

“…Little evidence clearly bearing on this hypothesis has subsequently appeared. In early work, a regenerative, spike-like depolarization was also reported in a few instances (O'Bryan, 1973;Fuortes, Schwartz & Simon, 1973). Later, found such spikes to be common in superfused, strontium-treated preparations and thereby highlighted the existence of both a 'transient' (spike) and 'sustained' (graded) feed-back depolarization.…”

“…In cones, however, the membrane potential can also be driven in the depolarizing direction. Thus, in various vertebrate species, the receptive field of the cone displays an antagonistic centre-surround organization: light in the centre evokes a hyperpolarizing response which can be reduced by light in the surround (Baylor et al 1971;O'Bryan, 1973;Burkhardt, 1977;Burkhardt, Hassin, Levine & MacNichol, 1980;Lasansky, 1981Lasansky, , 1984Lasater, 1982;Murakami, Shimoda, Nakatani, Miyachi & Watanabe, 1982;Skryzpek & Werblin, 1983;Perlman, Normann, Itzhaki & Daly, 1985;Byzov & Shura-Bura, 1986). The depolarization induced by light in the surround is generally believed to be mediated by a synaptic feed-back pathway from horizontal cells to cones (Baylor et al 1971;Piccolino & Gerschenfeld, 1977;Kaneko & Tachibana, 1986) and to play a functional role in aspects of spatial vision, light adaptation and colour vision.…”

“…To date, depolarizing responses evoked by stimulation of the receptive field surround have been most extensively studied in cones of the turtle, Pseudemys scripta elegans. Some years ago, O'Bryan (1973) reported complex effects of altering the cone's membrane potential. He therefore suggested that at least two separate graded depolarizing components contribute to the surround response.…”

Synaptic transmission at retinal ribbon synapses

“…O'Bryan (1973), Gerschenfeld and Piccolino (1980) and Burkhardt et al (1988) described Ca 2+ -dependent depolarizations which sometimes led to spikes in turtle cones, responses that were elicited by flashes of annular illumination in the presence of steady central illumination or by current injection into cones. Thoreson and Burkhardt (1990) found that the depolarizing responses in cones elicited by current injection were blocked by submicromolar concentrations of cobalt, suggesting that they depended on calcium.…”