Organization of synaptic inputs to paracerebral feeding command interneurons of Pleurobranchaea californica. I. Excitatory inputs

1. Neurons presynaptic to the phasic paracerebral feeding command interneurons (PC(p)'s) 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 PC(p)'s, while the accompanying paper reports inhibitory inputs. 2. 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 PC(p)'s and fires action-potential bursts in phase with PC(p) bursts during fictive feeding. 3. The class I electrotonic neuron (ET(I)) is a single, identified monopolar neuron per hemiganglion with a sparse dendritic arborization and no descending axon in the cerebrobuccal connective (CBC). The ET(I) is coupled with PC(p)'s only by means of a nonrectifying electrical synapse. Paradoxically, ET(I) receives opposite synaptic inputs from PC(p)'s and fires in antiphase with PC(p)'s during fictive feeding. 4. Class II electrotonic neurons (ET(II)'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 PC(p)'s by means of a nonrectifying electrical synapse. One of the ET(II)'s also delivers graded, long-latency polysynaptic chemical inputs to PC(p)'s. ET(II)'s have descending axons in the CBC, elicit fictive feeding when depolarized, and fire cyclically and in phase with PC(p)'s during fictive feeding. 5. 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 PC(p)'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 PC(p)'s during fictive feeding. 6. PSEs and Et(II)'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 PC(p)'s, share excitatory inputs with PC(p)'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.