Response sensitivity and voltage gain of the rod- and cone-horizontal cell synapses in dark- and light-adapted tiger salamander retina.

Abstract

1. Rods, cones, and horizontal cells (HCs) were recorded in superfused, flat-mounted isolated retinas of the larval tiger salamander, Ambystoma tigrinum, under dark- and light-adapted conditions. 2. Under dark-adapted conditions, HC responses to dim 500-nm light stimuli were mediated only by rods. In the linear voltage range (near the dark potentials), the average response to a light step of 0.5 s (500 nm, 0.438 photons per micron2 per s) was 0.41 +/- 0.06 (SD) mV for rods and 1.86 +/- 0.52 mV for HCs. The step sensitivity of rods was approximately 0.94 mV per photon micron2 s, or 0.032 mV per activated rhodopsin molecule (Rh*) rod second, and the step sensitivity of HCs was approximately 4.25 +/- 1.19 mV per photon micron2 s or 0.14 +/- 0.04 mV per Rh* rod second. The chord voltage gain of the rod-HC synapse had an average value of 4.54 and a range from 2.68 to 7.32. 3. By the use of the spectral subtraction method, we found that the average cone-mediated HC response to a 750-nm light step that elicited an average cone response of 0.73 +/- 0.20 mV was 1.15 +/- 0.31 mV. The step sensitivity of cones under dark-adapted conditions was 0.0012 mV per photon micron2 s, and that of the cone-mediated-HC response was 0.0019 mV per photon micron2 s. The chord voltage gains of the cone-HC synapses under dark-adapted conditions had an average value of 1.58 and a range from 0.82 to 2.05. 4. Under light-adapted conditions (with a 500-nm/-2.40 background light, which desensitized rod responses but did not substantially reduce the cone responses), the cones had an average response to a light step of 0.5 s (500 nm/-3.3) of 0.78 +/- 0.09 mV, and this response did not vary with time. The HC response to the same light step had an average value of 3.95 +/- 3.41 mV 3 min after the background light onset, and it increased with time until reaching a steady-state value of 5.95 +/- 3.63 mV approximately 15 min after the background light onset. The average chord voltage gain of the cone-HC synapse under such light-adapted conditions was 5.06 at 3 min after background light onset and 7.63 at 15 min after background light onset. These values are approximately 3-5 times higher than the chord voltage gain of the cone-HC synapse under dark-adapted conditions. 5. The background-induced increase of the chord voltage gain of the cone-HC synapse suggests that similarly to the rod-HC synapse, the voltage gain of the cone-HC synapse in the tiger salamander retina can also be modulated by light. Additionally, our results suggest that certain time-dependent process(es) in the synaptic cleft or postsynaptic membrane may be responsible for such modulation. 6. In addition to determining the average values of response sensitivity and chord voltage gains of the rod- and cone-HC synapses, we studied the variation of these parameters among different HCs. HCs with higher rod-HC synaptic gain had lower cone-HC synaptic gain, and HCs with lower rod-HC synaptic gain exhibited higher cone-HC synaptic gain under both dark- and light-adapted conditions. This suggests that the rod-HC and cone-HC synaptic gains in HCs are complementary to each other, and voltage responses of all HCs under dark- or light-adapted conditions are of comparable amplitudes.