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Volume 16, Number 13, Issue of July 1, 1996 pp. 4113-4128
Copyright ©1996 Society for Neuroscience

Cholinergic-Dependent Plateau Potential in Hippocampal CA1 Pyramidal Neurons

Received Feb. 27, 1996; revised April 2, 1996; accepted April 8, 1996.

Douglas D. Fraser and Brian A. MacVicar

Neuroscience Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4N1

Cholinergic stimulation of the hippocampal formation results in excitation and/or seizure. We report here, using whole-cell patch-clamp techniques in the hippocampal slice (34-35°C), a cholinergic-dependent slow afterdepolarization (sADP) and long-lasting plateau potential (PP). In the presence of 20 µM carbachol, action potential firing evoked by weak intracellular current injection elicited an sADP that lasted several seconds. Increased spike firing evoked by stronger depolarizing stimuli resulted in long-duration PPs maintained close to 20 mV. Removal of either Na⁺ or Ca²⁺ from the external media, intracellular Ca²⁺ ([Ca²⁺]_i) chelation with 10 mM bis(2-aminophenoxy)ethane-N,N,N,N-tetra-acetic acid, or the addition of 100 µM Cd²⁺ to the perfusate abolished both the sADP and PP. The sADP was depressed and the PP was abolished by either 10 µM nimodipine or 1 µM -conotoxin, whereas 1.2 µM tetrodotoxin was ineffective. The involvement of a Na⁺/Ca²⁺ exchanger was minimal because both the sADP and PP persisted after equimolar substitution of 50 mM Li⁺ for Na⁺ in the external media or reduction of the bath temperature to 25°C. Finally, in the absence of carbachol the sADP and PP could not be evoked when K⁺ channels were suppressed, suggesting that depression of K⁺ conductances alone was not sufficient to unmask the conductance. Based on these data, we propose that a Ca²⁺-activated nonselective cation conductance was directly enhanced by muscarinic stimulation. The sADP, therefore, represents activation of this conductance by residual [Ca²⁺]_i, whereas the PP represents a novel regenerative event involving the interplay between high-voltage-activated Ca²⁺ channels and the Ca²⁺-activated nonselective cation conductance. This latter mechanism may contribute significantly to ictal depolarizations observed during cholinergic-induced seizures.

Key words: muscarinic stimulation; Ca²⁺-activated nonselective cation conductance; HVA Ca²⁺ currents; ictal depolarization; epilepsy; slice-patch technique

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