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Intrinsic Excitability of Cholinergic Neurons in the Rat Parabigeminal Nucleus

¹Departments of Neurobiology and ²Neurology, Stanford University, Stanford, California

Submitted 26 August 2007; accepted in final form 25 September 2007

Cholinergic neurons in the parabigeminal nucleus of the rat midbrain were studied in an acute slice preparation. Spontaneous, regular action potentials were observed both with cell-attached patch recordings as well as with whole cell current-clamp recordings. The spontaneous activity of parabigeminal nucleus (PBN) neurons was not due to synaptic input as it persisted in the presence of the pan-ionotropic excitatory neurotransmitter receptor blocker, kynurenic acid, and the cholinergic blockers dihydro-beta-erythroidine (DHβE) and atropine. This result suggests the existence of intrinsic currents that enable spontaneous activity. In voltage-clamp recordings, I_H and I_A currents were observed in most PBN neurons. I_A had voltage-dependent features that would permit it to contribute to spontaneous firing. In contrast, I_H was significantly activated at membrane potentials lower than the trough of the spike afterhyperpolarization, suggesting that I_H does not contribute to spontaneous firing of PBN neurons. Consistent with this interpretation, application of 25 µM ZD-7288, which blocked I_H, did not affect the rate of spontaneous firing in PBN neurons. Counterparts to I_A and I_H were observed in current-clamp recordings: I_A was reflected as a slow voltage ramp observed between action potentials and on release from hyperpolarization, and I_H was reflected as a depolarizing sag often accompanied by rebound spikes in response to hyperpolarizing current injections. In response to depolarizing current injections, PBN neurons fired at high frequencies, with relatively little accommodation. Ultimately, the spontaneous activity in PBN neurons could be used to modulate cholinergic drive in the superior colliculus in either positive or negative directions.