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Ion Channel Compartments in Photoreceptors: Evidence From Salamander Rods With Intact and Ablated Terminals

Department of Anatomy and Neurobiology, Neuroscience Institute, Morehouse School of Medicine, Atlanta, Georgia

Submitted 27 July 2006; accepted in final form 16 April 2007

Vertebrate photoreceptors are highly polarized sensory cells in which several different ionic currents have been characterized. In the present study we used whole cell voltage-clamp and optical imaging techniques, the former combined with microsurgical manipulations, and simultaneous recording of membrane current and intracellular calcium signals to investigate the spatial distribution of ion channels within isolated salamander rods. In recordings from intact rods with visible terminals, evidence for five previously identified ionic currents was obtained. These include two Ca²⁺-dependent, i.e., a Ca²⁺-dependent chloride current [I_Cl(Ca)] and a large-conductance Ca²⁺- and voltage-dependent K⁺ or BK current [I_K(Ca)], and three voltage-dependent currents, i.e., a delayed-rectifier type current [I_K(V)], a hyperpolarization-activated cation current (I_h), and a dihydropyridine-sensitive L-type calcium current (I_Ca). Of these, I_Cl(Ca) was highly correlated with the presence of a terminal; rods with visible terminals expressed I_Cl(Ca) without exception (n = 125), whereas approximately 71% of rods (40/56) without visible terminals lacked I_Cl(Ca). More significantly, I_Cl(Ca) was absent from all rods (n = 33) that had their terminals ablated, and recordings from the same cell before and after terminal ablation led, in all cases (n =10), to the loss of I_Cl(Ca). In contrast, I_K(Ca), I_K(V), and I_h remained largely intact after terminal ablation, suggesting that they arose principally from ion channels located in the soma and/or inner segment. The outward I_K(Ca) in terminal-ablated rods was reversibly suppressed on "puffing" a Ca²⁺-free extracellular solution over the soma and was appreciably enhanced by the L-type Ca²⁺ channel agonist, Bay K 8644 (0.1–2 µM). These data indicate that rod photoreceptors possess discrete targeting mechanisms that preferentially sort ion channels mediating I_Cl(Ca) to the terminal.