scholarly journals Physiological roles of Na+/Ca2+ exchange in Limulus ventral photoreceptors.

1991 ◽  
Vol 97 (2) ◽  
pp. 369-391 ◽  
Author(s):  
P M O'Day ◽  
M P Gray-Keller ◽  
M Lonergan

In previous work we have presented evidence for electrogenic Na+/Ca2+ exchange in Limulus ventral photoreceptors (1989. J. Gen. Physiol. 93:473-492). This article assesses the contributions to photoreceptor physiology from Na+/Ca2+ exchange. Four separate physiological processes were considered: maintenance of resting sensitivity, light-induced excitation, light adaptation, and dark adaptation. (a) Resting sensitivity: reduction of [Na+]o caused a [Ca2+]o-dependent reduction in light sensitivity and a speeding of the time courses of the responses to individual test flashes; this effect was dependent on the final value to which [Na+]o was reduced. The desensitization caused by Na+ reduction was dependent on the initial sensitivity of the photoreceptor; in fully dark-adapted conditions no desensitization was observed; in light-adapted conditions, extensive desensitization was observed. (b) Excitation: Na+ reduction in fully dark-adapted conditions caused a Ca2+o-dependent depolarizing phase in the receptor potential that persisted beyond the stimulus duration and was evoked by a bright adapting flash. (c) Light adaptation: the degree of desensitization induced by a bright adapting flash was Na+o dependent, being larger with lower [Na+]o. Na+ reduction enhanced light adaptation only at intensities brighter than 4 x 10(-6) W/cm2. In addition to being Na+o dependent, light adaptation was Ca2+o dependent, being greater at higher [Ca2+]o. (d) Dark adaptation: the recovery of light sensitivity after adapting illumination was Na+o dependent. Dark adaptation after bright illumination in voltage-clamped and in unclamped conditions was faster in normal-Na+ saline than in reduced Na+ saline. The final sensitivity to which photoreceptors recovered was lower in reduced-Na+ saline when bright adapting illumination was used. The results suggest the involvement of Na+/Ca2+ exchange in each of these physiological processes. Na+/Ca2+ exchange may contribute to these processes by counteracting normal elevations in [Ca2+]i.

1973 ◽  
Vol 61 (3) ◽  
pp. 273-289 ◽  
Author(s):  
A. Fein ◽  
R. D. DeVoe

The early receptor potential (ERP), membrane potential, membrane resistance, and sensitivity were measured during light and/or dark adaptation in the ventral eye of Limulus. After a bright flash, the ERP amplitude recovered with a time constant of 100 ms, whereas the sensitivity recovered with an initial time constant of 20 s. When a strong adapting light was turned off, the recovery of membrane potential and of membrane resistance had time-courses similar to each other, and both recovered more rapidly than the sensitivity. The receptor depolarization was compared during dark adaptation after strong illumination and during light adaptation with weaker illumination; at equal sensitivities the cell was more depolarized during light adaptation than during dark adaptation. Finally, the waveforms of responses to flashes were compared during dark adaptation after strong illumination and during light adaptation with weaker illumination. At equal sensitivities (equal amplitude responses for identical flashes), the responses during light adaptation had faster time-courses than the responses during dark adaptation. Thus neither the photochemical cycle nor the membrane potential nor the membrane resistance is related to sensitivity changes during dark adaptation in the photoreceptors of the ventral eye. By elimination, these results imply that there are (unknown) intermediate process(es) responsible for adaptation interposed between the photochemical cycle and the electrical properties of the photoreceptor.


1988 ◽  
Vol 1 (4) ◽  
pp. 331-338 ◽  
Author(s):  
Cun-Jian Dong ◽  
Hao-Hua Qian ◽  
John S. McReynolds ◽  
Xiong-Li Yang ◽  
Yu-Min Liu

AbstractThe sensitivity of rod- and cone-driven responses was studied in the isolated frog retina during the period of rapid dark adaptation following a conditioning flash which bleached a negligible amount of visual pigment. Following a conditioning flash, cone-driven b-wave responses were first enhanced and then depressed. The time courses of the enhancement and subsequent depression of cone-drive responses varies greatly with the intensity and wavelength of the conditioning flash, but were identical when the conditioning' flashes were matched for equal excitation of 502 nm rods. These changes in cone-driven response sensitivity were correlated with the desensitization and recovery of rods following the conditioning flash. When signal transmission from rods to second-order cells was interrupted by the addition of L-glutamate, the conditioning flash did not produce the above-described enhancement and subsequent depression of long-wavelength receptor potential responses. The suppression of cone-driven response therefore appears to be due to a synaptically mediated influence from 502 nm rods which is maximal when the rods are in the dark-adapted state, with little or no contribution from 433 nm rods, and no involvement of the pigment epithelium.


1985 ◽  
Vol 85 (6) ◽  
pp. 805-841 ◽  
Author(s):  
S Levy ◽  
A Fein

The possible role of Ca ions in mediating the drop in sensitivity associated with light adaptation in Limulus ventral photoreceptors was assessed by simultaneously measuring the sensitivity to light and the intracellular free Ca concentration (Cai); the latter was measured by using Ca-selective microelectrodes. In dark-adapted photoreceptors, the mean resting Cai was 3.5 +/- 2.5 microM SD (n = 31). No correlation was found between resting Cai and absolute sensitivity from cell to cell. Typically, photoreceptors are not uniformly sensitive to light; the Cai rise evoked by uniform illumination was 20-40 times larger and faster in the most sensitive region of the cell (the rhabdomeral lobe) than it was away from it. In response to a brief flash, the Cai rise was barely detectable when 10(2) photons were absorbed, and it was saturated when approximately 10(5) photons were absorbed. During maintained illumination, starting near the threshold of light adaptation, steady Cai increases were associated with steady desensitizations over several log units of light intensity: a 100-fold desensitization was associated with a 2.5-fold increase in Cai. After a bright flash, sensitivity and Cai recovered with different time courses: the cell was still desensitized by approximately 0.5 log units when Cai had already recovered to the prestimulus level, which suggests that under those conditions Cai is not the rate-limiting step of dark adaptation. Ionophoretic injection of EGTA markedly decreased the light-induced Cai rise and increased the time to peak of the light response, but did not alter the resting Cai, which suggests that the time to peak is affected by a change in the capacity to bind Ca2+ and not by resting Cai. Lowering the extracellular Ca2+ concentration (Cao) first decreased Cai and increased sensitivity. Longer exposure to low Cao resulted in a further decrease of Cai but decreased rather than increased sensitivity, which suggests that under certain conditions it is possible to uncouple Cai and sensitivity.


1966 ◽  
Vol 49 (6) ◽  
pp. 1199-1208 ◽  
Author(s):  
WILLIAM L. PAK ◽  
THOMAS G. EBREY

The second phase (negative peak) of the early receptor potential of cones has been studied in the all-cone eyes of the Mexican and antelope ground squirrels (Citellus mexicanus and Citellus leucurus) and compared with responses from the rod-dominant eyes of the rat and flying squirrel (Glaucomys volans). The responses obtained from the all-cone eyes tended to be smaller in amplitude, to have higher thresholds, and to be considerably more resistant to light adaptation than the responses from the rod-dominant eyes. The wave forms and time courses of the two types of responses were similar, although the cone potential tended to be less sensitive to temperature variations and its time constants tended to be shorter than those of the rod potential. The spectral sensitivity of the second phase of the early receptor potential of the Mexican ground squirrel closely follows the absorption spectrum of a Dartnall nomogram pigment having its absorption maximum at 540 mμ. Moreover, as in the case of the rat, the amplitude of the response appears to be linearly related to the amount of pigment bleached in a flash. Thus, in both all-rod and all-cone systems the early receptor potential appears to arise in the photoexcitation of the respective visual pigment and appears to be closely linked to the initial photochemical events. The similarity of the wave form, time course, and stimulus-response curves in the two systems suggests that the early receptor potential is produced by similar mechanisms in all-rod and all-cone systems.


1986 ◽  
Vol 41 (5-6) ◽  
pp. 657-667 ◽  
Author(s):  
I. Claßen-Linke ◽  
H. Stieve

The time course of the recovery of the sensitivity of the Limulus ventral nerve photoreceptor was measured during dark adaptation following light adaptation by a bright 1 or 5 s illumination. The stimulus intensity ICR of a 300 μs light flash evoking a response of criterion amplitude (receptor potential or receptor current under voltage clamp conditions) was used as measure of sensitivity.The time course of dark adaptation shows two phases with time constants in the range of 5-9 s and 300-500 s (15 °C). Only the first of the two phases is significantly changed when the extracel- lular Ca2+-concentration is varied.The power function ICR = a·Io-tDA-b gives a good data fit for each of the two phases of dark adaptation. In the first phase the factor ax and the exponent bx are decreased when the external calcium is lowered from 10 mmol/1 to 250 μmol/1. Conversely a1 and b1 are increased when the Ca2+-concentration is raised to 40 mmol/1. For the second phase neither a2 nor b2 is changed significantly upon the changes in calcium concentration in the same experiments.The two phases of dark adaptation reflect the behaviour of the two components C1 and C2 of the electrical light response (receptor potential or receptor current). Under the conditions described here C, determines the size of the light response during the first phase of dark adaptation whereas C2 mainly influences the size of the response during the second phase.Interpretation: The fast first phase of dark adaptation is determined by the change in intracellu- lar Ca2+-concentration. The slower second phase of dark adaptation is not primarily calcium- controlled.


1983 ◽  
Vol 38 (11-12) ◽  
pp. 1043-1054 ◽  
Author(s):  
H. Stieve ◽  
M. Bruns ◽  
H. Gaube

Receptor potentials of Limulus ventral nerve photoreceptors were evoked in reproducible states of moderate light- and considerable dark adaptation (LA, DA) with light stimulus intensities from threshold to saturation values using a repeated flash sequence. With increasing light intensities latent period and time-to-peak shortened in the state of both LA and DA The decrease-time is prolonged by increasing stimulus intensities (LA and DA) and continues to rise even when the amplitude of the receptor potential is already saturated. The sigmoid response height vs. log stimulus intensity curve is shifted upon LA towards higher stimulus intensities, and its steepness is increased. LA prolongs latent period and time-to-peak at low light intensities; at high light intensities, however, the DA-values are longer. The decreasetime of the receptor potential is always shorter in the light-adapted state. The results are discussed according to the assumption that size and duration of the receptor potential are primarily determined by the distribution of bum p latencies. Changes of the receptor potential parameters are explained by changes of bum p size and of bum p latency distribution due to light adaptation.


1982 ◽  
Vol 99 (1) ◽  
pp. 61-90 ◽  
Author(s):  
DONALD H. EDWARDS

1. The responses of the cockroach descending contralateral movement detector (DCMD) neurone to moving light stimuli were studied under both light- and dark-adapted conditions. 2. With light-adaptation the response of the DCMD to two moving 2° (diam.) spots of white light is less than the response to a single spot when the two spots are separated by less than 10° (Fig. 2). 3. With light-adaptation the response of the DCMD to a single moving light spot is a sigmoidally shaped function of the logarithm of the light intensity (Fig. 3a). With dark-adaptation the response of a DCMD to a single moving light spot is a bell-shaped function of the logarithm of the stimulus intensity (Fig. 3b). The absolute intensity that evokes a threshold response is about one-and-a-half log units less in the dark-adapted eye than in the light-adapted eye. 4. The decrease in the DCMD's response that occurs when two stimuli are closer than 10°, and when a single bright stimulus is made brighter, indicates that lateral inhibition operates among the afferents to the DCMD. 5. It is shown that this inhibition cannot be produced by a recurrent lateral inhibitory network. A model of the afferent path that contains a non-recurrent lateral inhibitory network can account for the response/intensity plots of the DCMD recorded under both light-adapted and dark-adapted conditions. 6. The threshold intensity of the DCMD is increased if a stationary pattern of light is present near the path of the moving spot stimulus. This is shown to be due to a peripheral tonic lateral inhibition that is distinct from the non-recurrent lateral inhibition described earlier. 7. It is suggested that the peripheral lateral inhibition acts to adjust the threshold of afferents to local background light levels, while the proximal non-recurrent network acts to enhance the acuity of the eye to small objects in the visual field, and to filter out whole-field stimuli.


1980 ◽  
Vol 35 (3-4) ◽  
pp. 308-318 ◽  
Author(s):  
H. Stieve ◽  
I. Claßen-Linke

Abstract The electroretinogram (ERG) of the isolated retina of the crayfish Astacus leptodactylus evoked by strong 10 ms light flashes at constant 5 min intervals was measured while the retina was continuously superfused with various salines which differed in Ca2+ -and Na+ -concentrations. The osmotic pressure of test- and reference-saline was adjusted to be identical by adding sucrose. Results: 1. Upon raising the calcium-concentration of the superfusate in the range of 20-150 mmol/l (constant Na+ -concentration: 208 mmol/l) the peak amplitude hmax and the half time of decay t2 of the ERG both decrease gradually up to about 50% in respect to the corresponding value in reference saline. 2. The recovery of the ERG due to dark adaptation following the “weakly light adapted state” is greatly diminished in high external [Ca2+]ex. 3. Lowering the external calcium-concentration (10 →1 mmol/l) causes a small increase in hmax and a strong increase of the half time of decay t2 (about 180%). Upon lowering the calcium concentration of the superfusate to about 1 nmol/l by 1 mmol/l of the calcium buffer EDTA, a slowly augmenting diminution of the ERG height hm SLX occurs. How­ever, a strong retardation of the falling phase of the ERG characterized by an increase in t2 occurs quickly. Even after 90 min stay in the low calcium saline the retina is still not inexcitable; hmax is 5 - 10% of the reference value. The diminution of hmax occurs about six-fold faster when the buffer concentration is raised to 10 mmol/l EDTA. 4. Additional lowering of the Na+ -concentration (208 →20.8 mmol/l) in a superfusate with a calcium concentration raised to 150 mmol/l causes a strong reduction of the ERG amplitude hmax to about 10%. 5. In a superfusate containing 1 nmol/l calcium such lowering of the sodium concentration (208 → 20.8 mmol/l) causes a diminution of the ERG height to about 40% and the shape of the ERG to become polyphasic; at least two maxima with different time to peak values are observed. Interpretation: 1. The similarity of effects, namely raising external calcium concentration and light adaptation on the one hand and lowering external calcium and dark adaptation on the other hand may indicate that the external calcium is acting on the adaptation mechanism of the photoreceptor cells, presumably by influencing the intracellular [Ca2+]. 2. The great tolerance of the retina against Ca2+ -deficiency in the superfusate might be effected by calcium stores in the retina which need high Ca2+ -buffer concentrations in the superfusate to become exhausted. 3. In contrast to the Limulus ventral nerve photoreceptor there does not seem to be an antagonis­ tic effect of sodium and calcium in the crayfish retina on the control of the light channels. 4. The crayfish receptor potential seems to be composed of at least two different processes. Lowering calcium-and lowering external sodium-concentration both diminish the height and change the time course of the two components to a different degree. This could be caused by in­ fluencing the state of adaptation and thereby making the two maxima separately visible.


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