GUINEA-PIG VISCERAL C-FIBER NEURONS ARE DIVERSE WITH RESPECT TO THE K-POTENTIAL REPOLARIZATION( CURRENTS INVOLVED IN ACTION)

1. Intracellular recordings were made from C-fiber neurons identified by antidromic conduction velocity in intact guinea pig nodose ganglia maintained in vitro, and whole-cell patch clamp recordings were made f rom dissociated guinea pig nodose neurons to investigate the contribut ion of various K+ conductances to action-potentiaI repolarization. 2. The repolarizing phase of the intracellularly recorded action potentia l was prolonged in a concentration-dependent manner by charybdotoxin ( Chtx; EC(50) = 39 nM) or iberiatoxin( Ibtx; EC(50) = 48 nM) in a subpo pulation of 16/36 C-fiber neurons. In a subset of these experiments, r emoval of extracellular Ca2+ reversibly prolonged action-potential dur ation(APD) in the same 4/9 intracellularly recorded C-fiber neurons af fected by Chtx (greater than or equal to 100 nM). These convergent res ults support that a Ca2+ -activated K+ current (I-C) contributes to ac tion-potential repolarization in a restricted subpopulation of C-fiber neurons. 3. Tetraethylammonium (TEA; 1-10 mM) increased APD considera bly further in the presence of 100-250 nM Chtx or Ibtx, or in nominall y Ca2+-free superfusate in 14/14 intracellularly recorded C-fiber neur ons. TEA affected APD similarly in subpopulations of neurons with and without I-C, suggesting that a voltage-dependent K+ current (I-C) cont ributes significantly to action-potential repolarization in most nodos e C-fiber neurons. 4. Substitution of Mn2+ for Ca2+ reduced outward wh ole-cell currents elicited by voltage command steps positive to -30 mV (2-25 ms) in a subpopulation of 21/36 dissociated nodose neurons, sup porting the heterogeneous expression of I-C. The kinetics of outward t ail current relaxations (tau S Of 1.5-2 ms) measured at the return of 2-3 ms depolarizing steps to -40 mV were indistinguishable in neurons with and without I-C, precluding a separation of the nodose I-C and I- K by a difference in deactivation rates. 5. Chtx (10-250 nM) reduced i n a subpopulation of 3/8 C-fiber neurons the total outward current eli cited by voltage steps depolarized to -30 mV in single microelectrode voltage-clamp recordings. TEA (5-10 mM) further reduced outward curren t in the presence of 100-250 nM Chtx in all eight experiments. The Cht x-sensitive current was taken to represent I-C, and the TEA-sensitive current, the I-K component contributing to action-potential repolariza tion. 6. Rapidly inactivating current (I-A) was implicated in action-p otential repolarization in a subpopulation of intracellularly recorded C-fiber neurons. In 4/7 neurons, incremented hyperpolarizing prepulse s negative to -50 mV progressively shortened APD. The prepulse voltage -dependency of this effect was in accord with the steady-state inactiv ation voltage dependency for I-A measured directly from the same neuro ns in voltage-clamp. No I-A was evident in the three neurons in which the APD was not affected by the prepulse potential. 7. In conclusion, a diverse composite of K+ currents appears to control action-potential repolarization in nodose C-fiber neurons. Although a voltage-dependen t I-K may be ubiquitous, I-C or I-A appear to contribute in restricted subpopulations of neurons. Thisheterogeneity may reflect adaptation t o differing afferent functions subserved by these neurons.