A role for Ca2+ in excitation of retinal rods and cones

Hagins, W. A.; Yoshikami, S.

doi:10.1016/0014-4835(74)90157-2

Cited by 203 publications

(70 citation statements)

References 15 publications

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“…7, where the resolution of the Ca signal was good enough to allow the measurement of an increase in Ca; associated with a desensitization of 0.1 log unit, we estimate that 103_101 Ca ions are released per photoactivated rhodopsin within 60 s (assuming the volume of the R lobe to be 80 pl). This is very similar to what might be released from a vertebrate rod disk by one photon at threshold (Hagins and Yoshikami, 1974) .…”

Section: The Relationship Between the Light-induced Cai Increase And supporting

confidence: 71%

Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes.

Levy¹,

Fein²

1985

The Journal of General Physiology

101

106

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The possible role of Ca ions in mediating the drop insensitivity associated with light adaptation in Limulus ventral photoreceptors was assessed by simultaneously measuring the sensitivity to light and the intracellular free Ca concentration (Ca i) ; the latter was measured by using Ca-selective microelectrodes . In dark-adapted photoreceptors, the mean resting Cai was 3 .5 ± 2 .5,M 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^-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 Ca ; . After a bright flash, sensitivity and Cai recovered with different time courses : the cell was still desensitized by -0 .5 log units when Ca i 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 Ca;, which suggests that the time to peak is affected by a change in the capacity to bind Ca2' and not by resting Ca i . Lowering the extracellular Ca 21 concentration (Ca .) first decreased Cai and increased sensitivity. Longer exposure to low Ca. resulted in a further decrease of Ca ; but decreased rather than increased Address reprint requests to Dr.

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Section: The Relationship Between the Light-induced Cai Increase And supporting

confidence: 71%

Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes.

Levy¹,

Fein²

1985

The Journal of General Physiology

101

106

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“…7B). Divalent cations, such as Ca2+ and Ba2+ may directly block the cAMP-induced sodium inward current in neuron L5, as Ca2+ can block sodium channels in visual receptor cells of vertebrates (HAGINS and YOSHIKAMI, 1974), in horizontal cells isolated from goldfish retinae (TACHIBANA, 1985) and in the postsynaptic membrane of the crayfish muscle (ONODERA and TAKEUCHI, 1976). Aldenhoff and coworkers (ALDENHOFF et al, 1983) previously observed that in Helix neurons the cAMPinduced sodium inward current decreased when either [Ca2+]o or [Mg2+]o was raised.…”

Section: Discussionmentioning

confidence: 99%

Influences of pressure-injected cyclic AMP on the membrane current and characteristics of an identified neuron of Aplysia kurodai.

1985

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The ionic mechanism of the effect of intracellularly injected adenosine 3',5'-cyclic monophosphate (CAMP) on the membrane of identified neuron L5 of Apl ysia kurodai was investigated with conventional voltage-clamp and ion-substitution techniques. The intracellular elevation of CAMP caused an inward current ('CAMP), which was not accompanied by a significant change in membrane conductance at potentials more hyperpolarized than -60 mV. The current increased over the voltage range (-50 to -30 mV) associated with a conductance decrease and decreased at potentials more hyperpolarized than -60 mV. Elevated intracellular CAMP was found to enhance a region of negative slope resistance in steady-state I -V relations. Duration of the 'CAMP was greatly prolonged by bath-applied isobutylmethylxanthine (50 ,uM), but imidazole (10 mM) had an opposite effect on the 'CAMP. Tolbutamide (5 mM), a protein kinase inhibitor, reduced the DAMP. The current was not affected by the presence of bath-applied TTX (50 µM), ouabain (50 /LM), or triaminopyrimidine (5 mM). Reduction of [Na+]o reversibly decreased the DAMP. Li+ could largely substitute for Nat Alterations of [K+]o, and bath application of 4-AP (5 mM) and TEA (30 mM) did not affect the DAMP, In the presence of Nat, Cl-, and divalent cations such as Ca2+ and Ba2+ inhibited the DAMP. These results suggest that fast elevation of intracellular cAMP induces a TTX-resistant slow Na+ inward current, and the current might be due to activation of CAMP-dependent protein kinase.

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“…For example, bathing rods in low Ca2+ solutions in the presence of Na+ leads to a large increase in circulating current in darkness (Hagins & Yoshikami, 1974;Yau et al 1981). In low-Ca2 , O-Na+ solution, however, the circulating current is relatively stable.…”

Section: Extinction Of Background Illuminationmentioning

confidence: 99%

Cytoplasmic calcium as the messenger for light adaptation in salamander rods.

Fain

Lamb

Matthews

et al. 1989

The Journal of Physiology

146

184

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SUMMARY1. In order to study the role of cytoplasmic calcium concentration (Ca2+) in rod photoreceptor light adaptation, we have attempted to prevent light-induced changes in Ca 2' by minimizing calcium fluxes across the outer segment plasma membrane. This was achieved by exposing the outer segment to a low-Ca2 , 0-Na+ solution, in which sodium was replaced with either guanidinium or lithium and the external calcium concentration (Ca2+) was reduced to micromolar levels.2. With guanidinium and 1-3 ,sM-Cao , the circulating current in darkness was maintained for a period of at least 15 s, consistent with approximate stability of Ca 2+ With Li+ rather than guanidinium most of the initial current was suppressed, but the residual current was again relatively stable.3. During prolonged exposures (> 30 s) to low-Ca2 , 0-Na+ solution followed by dim illumination, the circulating current did not remain constant but slowly increased. Incorporation of calcium buffer into the cytoplasm greatly reduced the rate of change of current, consistent with the idea that the increase arose from a gradual decrease in Ca2+.4. Light responses of rods exposed to low-Ca2+, 0-Na+ solution in darkness were altered in a characteristic manner. Although the initial rising phase of the light response was little changed, the peak amplitude of the response was larger and occurred later, and the response decayed more slowly than in control. The response-intensity relation was steepened and was shifted towards lower intensities both for flashes and for steps of light. The normal sag in the response to steps disappeared, and the waveform of the step response could be predicted to a close approximation from the integral of the dim flash response.5. Presentation of background illumination in Ringer solution produced a marked acceleration of the response to a subsequent bright flash. No such acceleration was observed if the background was given in low-Ca2+, 0-Na+ solution.6. The results described in paragraphs 4 and 5 indicate that, under conditions expected to minimize changes in Ca2+, all manifestations of light adaptation disappear, and the rod simply sums the effects of incident photons with an invariant integration time.t To whom correspondence should be addressed. G. L. FAIN AND OTHERS7. Exposure of a light-adapted rod to low-Ca2 , 0-Na+ solution altered the responses to superimposed test flashes in much the same way as for rods in darkness. The initial rising phases in low-Ca2+, 0-Na+ solution were unchanged, but the responses were larger, reached peak later and decayed more slowly. Nevertheless, when the low-Ca2+, 0-Na+ solution was presented on adapting backgrounds of increasing intensity, the time-to-peak of responses shortened in a graded manner.8. Extinction of the background in low-Ca2 , 0-Na+ solution elicited large lightsuppressible currents, presumably as a result of increased cytoplasmic cyclic GMP concentration. The rate of increase of these currents was graded with the intensity of the prior background.9. The results described in para...

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A role for Ca2+ in excitation of retinal rods and cones

Cited by 203 publications

References 15 publications

Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes.

Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes.

Influences of pressure-injected cyclic AMP on the membrane current and characteristics of an identified neuron of Aplysia kurodai.

Cytoplasmic calcium as the messenger for light adaptation in salamander rods.

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