Localization and function of the electrical oscillation in electroreceptive ampullary epithelium from skates

A steady, spontaneous current oscillation (1 nA p-p) occurs in voltage-clamped, isolated ampullary organs (canal, ampulla, and nerve) from skates (Raja). Spectral analysis showed that energy in the oscillation was confined to a narrow band of frequencies (3 Hz) about a fundamental frequency (32 Hz at 20 degrees C) and in harmonics. The frequency of the oscillation was temperature dependent (increasing from 21 to 33 Hz for increases in temperature from 13 degrees C to 21 degrees C). The addition of 0.5 microM tetrodotoxin to the basal side of the ampullary epithelium eliminated afferent nerve activity but had no effect on the epithelial oscillation, indicating that the oscillation is not generated or induced by afferent nerve activity. Nitrendipine (2 microM) added to the solution bathing the basal side of the ampullary epithelium abolished the oscillation rapidly (within minutes), but a steady-state negative conductance (i.e., real part of the complex admittance < 0) generated by the preparation remained for 36 min. Conversely, nitrendipine (50 microM) added to the perfusate (artificial sea water) of the apical side eliminated the negative conductance rapidly (18.5 min) but had no effect on the spontaneous oscillation for more than 1 h. The effect and the elapsed time for an effect of nitrendipine after separate applications to the basal and apical membrane surfaces of ampullary epithelium suggest that 1) the negative conductance and the oscillation are generated independently in apical and basal membranes, respectively, and 2) both processes involve L-type Ca channels. Furthermore, the addition of tetraethylammonium (2 mM) to the basal side eliminated both the oscillation and the postsynaptic response to voltage clamps (< or = 100 microV) of the ampullary epithelium in the operational voltage range of the afferent nerve. This result suggests that the basal membrane oscillation functions in neurotransmitter release from presynaptic (basal) membranes.