Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat

Abstract

Neurons in the substantia nigra pars reticulata and pars compacta of the rat were studied using a combination of intracellular electrophysiological recording in in vitro and subsequent immunocytochemical double and triple labelling techniques. The neurons recorded in the pars reticulata were identified as either GABA or dopamine neurons: neurons were considered to be GABA neurons if they were immunopositive for glutamate decarboxylase, whereas those neurons which were immunopositive for tyrosine hydroxylase were considered to be dopaminergic. The GABA neurons had short duration action potentials (0.45±0.03 ms halfwidth), no apparent rectifying currents, no low threshold calcium spikes, were spontaneously active (7.4±3.7 Hz), and could maintain high firing rates. The dopamine neurons had long duration action potentials (1.49±0.10 ms), displayed both anomalous inward and transient outward rectifying currents, and more than half (12/17 neurons) displayed a low threshold calcium spike. Their spontaneous firing rate was lower than that of the GABA neurons (2.3±1.0 Hz), and they displayed strong frequency adaptation. Morphological reconstruction of neurobiotin-filled neurons revealed that the pars reticulata GABA neurons had more extensive local dendritic arborization than the dopamine neurons from either the pars reticulata or the pars compacta. All of the neurons recorded from the pars compacta were dopamine neurons; they were found not to be different either electrophysiologically or morphologically from pars reticulata dopamine neurons. The electrophysiology of the GABA neurons suggests that input activity is translated linearly to spike frequency. These GABA neurons probably represent the projection neurons of the pars reticulata, and it is thus likely that this basal ganglia output is frequency coded. The close similarity between the dopamine neurons in the pars compacta, which give rise to the nigrostriatal pathway, and those in the pars reticulata supports the notion that the dopamine neurons in these two regions are part of the same neuronal population.