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Microscopic heterogeneity in unitary N‐type calcium currents in rat sympathetic neurons.

1. Single N‐type calcium (Ca2+) channels in rat superior cervical ganglion neurons display complex patterns of activity in both inactivating and non‐inactivating gating modes. Unitary currents were elicited by holding the patch at ‐90 mV and stepping to +30 mV for 740 ms. Barium (110 mM) was used as the charge carrier. The dihydropyridine agonist (+)‐202‐791 was included in the bath to ensure that single channel recordings showed no L‐type Ca2+ channel mode 2 activity. Using this protocol, we characterized three additional patterns of N‐type Ca2+ channel activity named: (1) LLP for large unitary current amplitude (i = ‐0.92 pA) and low open probability (Po = 0.26); (2) SLP for small unitary current amplitude (i = ‐0.77 pA) and low open probability (Po = 0.25); and (3) SHP for its small unitary current (i = ‐0.77 pA) and higher open probability (Po = 0.39). 2. Transitions among these patterns of activity occur more slowly than transitions between closed and open states, resulting in significant clustering of like sweeps. Thus, the complicated gating of single N‐type Ca2+ channels can be dissected into multiple, independent modes, each with the same reproducible pattern of activity. 3. This heterogeneous activity is not unique to sympathetic neurons, for inactivating (4), non‐inactivating (4), SLP (4) and SHP (3 patches) gating modes were also observed in cell‐attached patch recordings (n = 4) of single N‐type Ca2+ channels in differentiated phaeochromocytoma (PC12) cells. 4. The 1568 sweeps from four single N‐type Ca2+ channel recordings that used the same voltage protocol were categorized by mode to determine the frequency of occurrence of each. Of the 54% of sweeps that showed activity, 42% were inactivating and 58% were non‐inactivating. The contribution by each mode to the sustained current was estimated using the equation: I = NPoi, where N is the frequency of occurrence of each mode and Po and i are the mean values of open probability and unitary current amplitude respectively. The LLP mode contributed 18%, the SLP mode 16%, and the SHP mode 66% of the sustained whole cell N‐type Ba2+ current. 5. The variability in the incidence among these modes in other cell types may resolve some of the controversy surrounding the characterization of N‐ and L‐type whole cell Ca2+ current components in peripheral neurons. In addition, the number of different modes provides a source of plasticity that may be a target of modulation by neurotransmitters and cellular signals.