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In the preceding paper (Arbas and Calabrese, 1987), we identified several properties that contribute to the activity of neurons (HN cells) that control heartbeat in the medicinal leech. Premotor HN (7) interneurons, which do not generate the heartbeat rhythm, exhibit Na+- dependent fast action potentials, Ca2+-mediated plateau potentials in the absence of Na+, and hyperpolarization-activated “restorative” changes in membrane potential that depolarize the membrane potential on hyperpolarization due to injected currents or synaptic inhibition. HN interneurons of ganglia 3 and 4 (i.e., timing oscillator interneurons) exhibit all of the properties described for HN (7) interneurons and have the additional characteristic that they are connected in oscillatory circuits. Reciprocal oscillations in membrane potential occurred in the bilateral HN interneurons (3) and (4) in the presence of elevated Ca2+ that were independent of Na+ -mediated action potentials. Their ability to oscillate in this way is based on 3 parameters: (1) production of a regenerative plateau potential by one of the pair of HN neurons in either ganglion, (2) inhibition of the contralateral HN neuron by the HN neuron in plateau, and (3) a phase transition mediated by escape from inhibition by the hyperpolarized HN neuron. The conductances responsible for restorative membrane potential shifts activated by hyperpolarization during synaptic inhibition may mediate the escape from inhibition that times the phase transition of the 2 HN neurons.

Slow oscillations of membrane potential in interneurons that control heartbeat in the medicinal leech