The Journal of Neurophysiology Vol. 79 No. 6 June 1998, pp. 3012-3018
Copyright ©1998 The American Physiological Society

Calcium-Sensitive Calcium Influx in Photoreceptor Inner Segments

William H. Baldridge, Dmitri E. Kurennyi, and Steven Barnes

Neuroscience Research Group, University of Calgary, Faculty of Medicine, Calgary, Alberta T2N 4N1, Canada

Baldridge, William H., Dmitri E. Kurennyi, and Steven Barnes. Calcium-sensitive calcium influx in photoreceptor inner segments. J. Neurophysiol. 79: 3012-3018, 1998. The effect of external calcium concentration ([Ca²⁺]_o) on membrane potential-dependent calcium signals in isolated tiger salamander rod and cone photoreceptor inner segments was investigated with patch-clamp and calcium imaging techniques. Mild depolarizations led to increases in intracellular Ca²⁺ levels ([Ca²⁺]_i) that were smaller when [Ca²⁺]_o was elevated to 10 mM than when it was 3 mM, even though maximum Ca²⁺ conductance increased 30% with the increase in [Ca²⁺]_o. When external calcium was lowered to 1 mM [Ca²⁺]_o, maximum Ca²⁺ conductance was reduced, as expected, but the mild depolarization-induced increase in [Ca²⁺]_i was larger than in 3 mM [Ca²⁺]_o. In contrast, when photoreceptors were strongly depolarized, the increase in [Ca²⁺]_i was less when [Ca²⁺]_o was reduced. An explanation for these observations comes from an assessment of Ca²⁺ channel gating in voltage-clamped photoreceptors under changing conditions of [Ca²⁺]_o. Although Ca²⁺ conductance increased with increasing [Ca²⁺]_o, surface charge effects dictated large shifts in the voltage dependence of Ca²⁺ channel gating. Relative to the control condition (3 mM [Ca²⁺]_o), 10 mM [Ca²⁺]_o shifted Ca²⁺ channel activation 8 mV positive, reducing channel open probability over a broad range of potentials. Reducing [Ca²⁺]_o to 1 mM reduced Ca²⁺ conductance but shifted Ca²⁺ channel activation negative by 6 mV. Thus the intracellular calcium signals reflect a balance between competing changes in gating and permeation of Ca²⁺ channels mediated by [Ca²⁺]_o. In mildly depolarized cells, the [Ca²⁺]_o-induced changes in Ca²⁺ channel activation proved stronger than the [Ca²⁺]_o-induced changes in conductance. In response to the larger depolarizations caused by 80 mM [K⁺]_o, the opposite is true, with conductance changes dominating the effects on channel activation.

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