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

Abstract

Neurons presynaptic to the phasic paracerebral feeding command interneurons (PCP's; Ref. 55) of Pleurobranchaea were located in the isolated central nervous system (CNS) and studied anatomically by lucifer yellow injection and physiologically by current injection and intracellular recording in normal and ion-substituted seawater during quiescence and fictive feeding. The present paper describes excitatory inputs to PCP's, while the accompanying paper (54) reports inhibitory inputs. Monosynaptic excitors (MSEs) are a group of at least three monopolar neurons per hemiganglion. Two have similar dendritic structures and functional effects. Each MSE monosynaptically excites the PCP's and fires action-potential bursts in phase with PCP bursts during fictive feeding. The class I electrotonic neuron (ETI) is a single, identified monopolar neuron per hemiganglion with a sparse dendritic arborization and no descending axon in the cerebrobuccal connective (CBC). The ETI is coupled with PCP's only by means of a non-rectifying electrical synapse. Paradoxically, ETI receives opposite synaptic inputs from PCP's and fires in antiphase with PCP's during fictive feeding. Class II electrotonic neurons (ETII's) are a group of at least two identified multipolar neurons per hemiganglion with indistinguishable dendritic architectures and similar but distinguishable functional effects. Each cell is coupled with PCP's by means of a nonrectifying electrical synapse. One of the ETII's also delivers graded, long-latency poly-synaptic chemical inputs to PCP's. ETII's have descending axons in the CBC, elicit fictive feeding when depolarized, and fire cyclically and in phase with PCP's during fictive feeding. Polysynaptic excitors (PSEs) are a group of at least two identified monopolar neurons per hemiganglion with similar elaborate dendritic fields and functional effects. Each cell excites PCP's by a long-latency, relatively nongraded polysynaptic pathway. PSEs also have descending axons in the ipsilateral CBC, elicit fictive feeding when depolarized, and fire in phase with PCP's during fictive feeding. PSEs and ETII's are here recognized as subclasses of neurons previously identified as paracerebral neurons. They are inhibited by the same neurons that supply recurrent inhibition to PCP's (47), share excitatory inputs with PCP's, and exhibit a similar "command" capacity. This study thus documents redundancy and functional specialization within a command system controlling a relatively complex rhythmic motor behavior.