Organization of synaptic inputs to paracerebral feeding command interneurons of Pleurobranchaea californica. II. Inhibitory inputs

Central neurons that deliver inhibitory synaptic inputs to the phasic paracerebral feeding command interneurons (PCp'S) in the cerebropleural ganglion of the mollusk Pleurobranchaea were studied anatomically and electrophysiologically, as in the preceding paper (11). The following inhibitory neurons have been located in each hemiganglion. Monosynaptic inhibitors (MSIs) are a population of three identified neurons on the dorsal surface of each cerebropleural hemiganglion. Each displays a distinct and repeatable dendritic architecture. The physiological effects of all three cells are similar, however. Each produces a small (1-2 mV) inhibitory postsynaptic potential (IPSP) with short and constant latency in phasic PCp'S. Trains of MSI action potentials at physiological discharge frequencies silence PCp'S. During fictive feeding the MSIs fire bursts of action potentials in approximate antiphase with PCp bursts. Dorsal medial polysynaptic inhibitors (PSI(DM'S)) are a class of three identified neurons per hemiganglion, each with a distinct dendritic architecture but similar physiological features. Each causes a long and variable latency (1-2s) barrage of IPSPs in PCp'S. At least some of these cells inhibit both ipsi- and contralateral PCp'S. The PSI(DM'S) are active cyclically during fictive feeding but the phase relationship was paradoxically variable through 180°. Ipsilateral and contralateral PSI(DM'S) are excitatorily coupled. The dorsal lateral polysynaptic inhibitor (PSI(DL)) is a single, identified bipolar neurons per hemiganglion with physiological effects similar to the aforementioned polysynaptic inhibitors. The PSI(DL) paradoxically fires in phase with PCp'S during fictive feeding, and its synaptic inputs are organized to effect this discharge pattern. The ventral anterior polysynaptic inhibitor (PSI(VA)) is a single, identified monopolar neuron per hemiganglion that elicits a long and variable latency (1-2 s) barrage of compound TPSPs in PCp'S. The neuron fires in antiphase with PCp'S but, as shown by hyperpolarization, is not necessary to the cyclic inhibition of PCp'S that normally occurs during rhythmic buccal motor output. The ventral posterior polysynaptic inhibitors (PST(VP'S) are at least two electrically coupled neurons per hemiganglion with a similar monopolar or weakly bipolar morphology and similar physiological effect. Stmulation of PSI(VP) causes a long-lasting train of compound IPSPs in PCp'S that can outlast the stimulus. The PSI(VP'S) fire in antiphase with phasic PCp'S during electrically induced rhythmic buccal motor output. Hyperpolarization of PSI(VP'S) during rhythmic buccal motor output reduces the cyclic inhibition of PCp'S that normally occurs during fictive feeding and, hence, PSI(VP'S) are at least partially necessary to this cyclical hyperpolarization. Known excitatory and inhibitory inputs to the paracerebral command neurons are summarized in a circuit diagram of the synaptic organization of this command system. The five major organizational features of this system are excitation of the feeding behavior by the command interneurons, excitation of a recurrent cyclical inhibitory network by the command interneurons, inhibition by the same network of central excitatory inputs to the command interneurons, interactions between neurons presynaptic to the command interneurons, and excitation of both the command interneurons and their cylical inhibitory inputs by sensory influences.