Physiological and kinetic properties of cholinergic receptors activated by multiaction interneurons in buccal ganglia of Aplysia

Abstract

1. Neurons of Aplysia buccal ganglia contain three types of acetylcholine (ACh) receptors, each of which has been characterized by its sensitivity to inhibitors and kinetics of desensitization and by the properties of the conductance change it controls, including reversal potential, major ion, and functional consequence. The receptors are classified as depolarizing, slowly decrementing hyperpolarizing, and rapidly decrementing hyperpolarizing. Identified neurons are innervated by identified cholinergic multiaction interneurons; the form of the postsynaptic potential produced depends on the number and class of receptor found on each cell. 2. Interneuronal action potentials produce monosynaptic IPSPs by activating slowly decrementing hyperpolarizing receptors on seven cells in each ganglion. The IPSP reversal potential of 75 mV is shifted 42 mV in a depolarizing direction in Cl = free seawater. The ACh response has a reversal potential identical to that of the PSP; the PSP is blocked by 10(-4) g/ml curare but unaffected by hexamethonium. Interneuronal action potentials also produce monosynaptic EPSPs with a -14 mV extrapolated reversal potential by activating depolarizing receptors on one cell in each ganglion. This PSP is blocked by 10(-4) g/ml hexamethonium and mimicked by a Na-dependent ACh response. 3. Each interneuronal action potential also produces a diphasic depolarizing-hyperpolarizing synaptic potential in one cell in each ganglion as a result of released ACh acting on two classes of postsynaptic receptor on the same cell. One of these receptors is depolarizing; the other is a rapidly decrementing hyperpolarizing receptor. The two differ in their sensitivity to inhibitors, and the conductance changes they produce differ in their reversal potential, duration, and functional consequences. Both components can be mimicked by iontophoretic application of ACh. 4. Although the hyperpolarizing receptors on the inhibitory and diphasic follower cells have similar sensitivity to inhibitors and control similar conductance changes, they differ in their kinetics of desensitization. The hyperpolarizing receptor on the diphasic cell shows marked decrement to repeated presynaptic action potentials and to repeated iontophoretic application of ACh. This decrement is greater than that seen in either the hyperpolarizing receptor on the inhibitory follower cell or the depolarizing receptor on the dual follower cell. The shape of the PSP in the diphasic follower and its effect on firing of the cell are thus functions of both membrane potential and the degree of desensitization of the receptor. 5. Rate of desensitization is, therefore, an additional criterion for characterizing otherwise similar receptors for neurotransmitters.