The Photovoltage of Macaque Cone Photoreceptors: Adaptation, Noise, and Kinetics

Abstract

Whole-cell voltage and current recordings were obtained from red and green cone photoreceptors in isolated retina from macaque monkey. It was demonstrated previously that the cone photovoltage is generated from two sources, phototransduction current in the cone outer segment and photocurrent from neighboring rods. Rod signals are likely transmitted to cones across the gap junctions between rods and cones. In this study, the "pure" cone and rod components of the response were extracted with rod-adapting backgrounds or by subtracting the responses to flashes of different wavelength equated in their excitation of either rods or cones. For dim flashes, the pure cone component was similar in waveform to the cone outer segment current, and the rod component was similar to the photovoltage measured directly in rods. With bright flashes, the high frequencies of the rod signal were filtered out by the rod/cone network. The two components of the cone photovoltage adapted separately to background illumination. The amplitude of the rod component was halved by backgrounds eliciting ϳ100 photoisomerizations sec Ϫ1 per rod; the cone component was halved by backgrounds of 8700 photoisomerizations sec Ϫ1 per cone. Coupling between rods and cones was not modulated by either dim backgrounds or dopamine. Voltage noise in dark-adapted cones was dominated by elementary events other than photopigment isomerizations. The dark noise was equivalent in magnitude to a steady light eliciting ϳ3800 photoisomerizations sec Ϫ1 per cone, a value significantly higher than the psychophysical estimates of cone "dark light." Key words: rod; cone; photoreceptor; primate; adaptation; couplingCertain aspects of human vision, such as color sensitivity, are determined by the process of light absorption and phototransduction in cone outer segments Schnapf et al., 1987). But other aspects of vision, such as temporal sensitivity and light adaptation, cannot be explained by properties of the outer segment and must therefore be determined principally by processes downstream (Schnapf et al., 1990). The first downstream locus of signal processing in the retina is the photoreceptor inner segment. Here the photocurrent is shaped by voltageactivated conductances (Barnes, 1994) and combined with synaptic inputs from neighboring neurons (Baylor et al., 1971). The purpose of the present work was to understand how the cone inner segment modifies the photocurrent and how these modifications affect vision. To address these questions, we recorded photovoltage from cone inner segments in freshly isolated retina from macaque monkeys.Psychophysicists describe two distinct retinal mechanisms by which rod signals are processed in parallel. One mechanism is slow and sensitive to dim light, and the second is faster and operates at mesopic light levels (Conner and MacLeod, 1977;Conner, 1982). It has been suggested that the rod-to-bipolar synapse connects rods to the more sensitive mechanism and that gap junctional coupling between rods and cones connects rods to the second mech...

Regulation of ON bipolar cell activity

“…In mouse, rod bipolar cells each receive input from about 22 rods, while cone bipolar cells gather input from 4-7 cones (Tsukamoto et al, 2001). Furthermore, the integration time of mammalian cones is about 25 msec (Schneeweis and Schnapf, 1999), underlying the cone pathway's ability to respond at higher temporal frequencies compared with the rod pathway. Assuming a Ca 2+ feedback system with the same time constant of recovery of 375 ms, as has been measured in rods (Berntson et al, 2004a), then the time required to recover from even a brief light stimulus would strongly compromise the sensitivity of cone bipolar cells for an order of magnitude longer than the integration time of the cone.…”

Gap-Junctional Coupling and Absolute Sensitivity of Photoreceptors in Macaque Retina

“…The fast component arises primarily from phototransduction in cone outer segments Schnapf, 1995, 1999). The slow component arises from phototransduction in rods that are coupled to the cone through gap junctions (Schneeweis and Schnapf, 1995Schnapf, , 1999 and is the subject of this study. Rod signals were evident in 90% of the red and green cones recorded (n ϭ 144), with no observed differences between the two cone types.…”

“…To compare rod and cone responses in detail, we recorded photovoltages in response to flashes of 500 nm light that evoked on average between 0.25 and 2.0 R*/rod. At these low light levels, the contribution of cone phototransduction to the cone photovoltage is negligible (Schneeweis and Schnapf, 1999). In part, the trial-to-trial variability in response amplitude reflects fluctuations in the number of photons absorbed (Baylor et al, 1979;Schneeweis and Schnapf, 1995).…”

Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression

“…and between cones of different classes (Schneeweis and Schnapf, 1999;Rieke and Baylor, 2000;Burns and Baylor, 2001;Sampath and Baylor, 2002;Ala-Laurila et al, 2004;Dunn and Rieke, 2006;Nikonov et al, 2006).…”

“…The rationale for this choice is that contrast weights are invariant with respect to changes in the chromaticity and intensity of the background if photoreceptors adapt according to Weber's Law (i.e., gain for each class of receptor inversely proportional to background isomerization rate for that class). Weber's Law provides a reasonable first-order description of photoreceptor adaptation over much but not all of their operating range (Demontis et al, 1993;Schneeweis and Schnapf, 1999). Indeed, if Weber's Law adaptation perfectly described the behavior of the coupling between photoreceptors and postreceptoral neurons, the relative contributions of rods and cones would not change with background intensity when expressed as contrast weights.…”