ELECTROPHYSIOLOGY OF DOPAMINERGIC AND NONDOPAMINERGIC NEURONS OF THE GUINEA-PIG SUBSTANTIA-NIGRA PARS COMPACTA INVITRO

1. The membrane properties of substantia nigra pars compacta neurones were studied using an in vitro slice preparation of guinea-pig midbrain. 2. Neurones were divided into two classes based on their electrophysiological properties: bursting neurones displayed a burst of several rapidly accommodating action potentials in response to relaxation of hyperpolarizing current injected through the microelectrode, while non-bursting neurones produced regularly spaced action potentials. These neuronal types were found to be electrophysiologically distinct from those recorded in the substantia nigra pars reticulata and the subthalamic nucleus. 3. Non-bursting neurones, which comprised ca 85% of the sampled cells, were characterized by a slow, pacemaker pattern of firing at rest, broad action potentials, a pronounced spike after-hyperpolarization, long membrane time constants, and strong transient outward and time-dependent inward rectification. 4. Bursting neurones, comprising ca 15% of the sample, displayed rapid firing rates at rest, fast action potentials, a shallow spike after-hyperpolarization and briefer membrane time constants. All of these parameters were significantly different from those of the non-bursting type. Bursting neurones lacked transient outward or time-dependent inward rectification. 5. Both types of cells were capable of generating pronounced calcium-dependent, low-threshold spikes in the presence of tetrodotoxin (TTX). However, only the non-bursting type displayed calcium-dependent rhythmic oscillations in membrane potential near resting potential in the presence of TTX. The firing rate, action potential shape and after-hyperpolarization of non-bursting neurones were strongly influenced by calcium-dependent currents. 6. The majority of cells were injected with biocytin, which allowed morphological reconstruction of the neurones and confirmation of their location within the pars compacta. Non-bursting neurones had variable soma shapes and their dendrites were mostly directed in a medio-lateral direction. Many cells extended some of their dendrites into the pars reticulata. Bursting neurones were mainly fusiform in shape with their dendrites oriented in a medio-lateral direction; a few had dendrites extending into the pars reticulata. 7. Thirty-six neurones were also double labelled using a combination of biocytin or Lucifer Yellow injection with tyrosine hydroxylase (TH) immunohistochemistry. Non-bursting neurones all displayed TH immunofluorescence, while none of the bursting neurones were TH positive. 8. Bursting neurones were found predominantly in the dorsal part of the rostral pars compacta, while non-bursting cells were found throughout. The distribution of bursting neurones paralleled the distribution of glutamic acid decarboxylase (GAD)-immunoreactive neurones in the pars compacta. 9. These results strongly suggest that non-bursting cells are dopaminergic, while bursting cells are non-dopaminergic, and probably GABAergic. Possible functional correlates of these cell types are discussed.