Intracellular and extracellular electrophysiology of nigral dopaminergic neurons--3. Evidence for electrotonic coupling.

Using three independent in vivo methods, we have obtained evidence for electrotonic coupling between sets of rat zona compacta dopaminergic neurons: (1) Lucifer yellow injection into single dopamine neurons resulted in labeling of two to five dopamine neurons in 18 out of 33 injections. Similar injections into reticular formation or nigral reticulata cells did not demonstrate multiple labeling. (2) Intracellular recording revealed spontaneously occurring small (3-15 mV) fast potentials that often triggered action potentials in dopamine neurons when the membrane potential was close to firing threshold. These fast potentials had a firing rate and pattern similar to that reported previously for extracellularly recorded dopamine neurons. Fast potentials were activated antidromically from the caudate nucleus at a latency similar to that reported for dopamine neurons, followed high frequency antidromic stimulation at a constant latency, and collided with spontaneously occurring fast potentials. However, directly elicited action potentials would not collide reliably with antidromically activated fast potentials. Intracellular injection of depolarizing or hyperpolarizing current increased and decreased, respectively, the rate of occurrence of these potentials. The firing rate of fast potentials could be increased and decreased by the intravenous administration of dopamine antagonists and agonists, respectively. (3) Simultaneous extracellular recording from pairs of DA neurons revealed numerous instances of synchronized action potentials. This was observed more frequently following intravenous haloperidol administration. Sets of burst firing dopamine neurons recorded simultaneously consistently demonstrated a decrease in the interspike interval as the burst progressed; a phenomenon commonly reported in other electrically coupled systems. Electrical coupling has been suggested to be present in sets of identified nigrostriatal dopamine neurons. Electrical communication between these neurons could be involved in modulating burst firing and in synchronizing dopamine release.