Ionic basis of tonic firing in spinal substantia gelatinosa neurons of rat

Ionic conductances underlying excitability in tonically firing neurons (TFNs) from substantia gelatinosa (SG) were studied by the patch-clamp method in rat spinal cord slices. Ca2+-dependent K+ (K-CA) conductance sensitive to apamin was found to prolong the interspike intervals and stabilize firing evoked by a sustained membrane depolarization. Suppression of Ca2+ and K-CA currents, however, did not abolish the basic pattern of tonic firing, indicating that it was generated by voltage-gated Na+ and K+ currents. Na+ and K+ channels were further analyzed in somatic nucleated patches. Na+ channels exhibited fast activation and inactivation kinetics and followed two-exponential time course of recovery from inactivation. The major K+ current was carried through tetraethylammonium (TEA)-sensitive rapidly activating delayed-rectifier (K-DR) channels with a slow inactivation. The TEA-insensitive transient A-type K+ (K-A) current was very small in patches and was strongly inactivated at resting potential. Block of K-DR rather than K-A conductance by 1 mM TEA lowered the frequency and stability of firing. Intracellular staining with biocytin revealed at least three morphological groups of TFNs. Finally, on the basis of present data, we created a model of TFN and showed that Na+ and K-DR currents are sufficient to generate a basic pattern of tonic firing. It is concluded that the balanced contribution of all ionic conductances described here is important for generation and modulation of tonic firing in SG neurons.