Electric fields were applied to study the regenerative properties of substantia nigra pars compacta neurons in guinea-pig brain slices. Two types of spikes, of high or low amplitude, were generated in both the soma-hyperpolarizing and the soma-depolarizing directions of the field. The different sensitivity of the spikes to somatic polarization suggested that the high-amplitude spikes were generated near the cell body, whereas the low-amplitude spikes were generated at a distance from the soma. Application of tetrodotoxin or intracellular injection of QX 314 abolished both types of spike. The spikes were not inhibited in the presence of glutamate receptor antagonists or during Ca2+ channel blockade. Blockers of gap junctional conductance (sodium propionate, octanol and halothane) did not affect the field-induced spikes. The spike generation was highly sensitive to changes in membrane conductance induced by current injection in the soma or by external field application. The ability of a conditioning field stimulation to affect the spike generation in different neuronal compartments suggested that a transient outward current was generated in the dendrites. The field-induced spikes were facilitated by synaptic stimulation and, in some neurons, low-amplitude spikes were generated by synaptic potentials in the absence of field application. These results suggest that channels responsible for Na+ spike generation reside in the dendrites, and are influenced by spatially distributed voltage-dependent K+ currents and by synaptic input.