Control of extrinsic feeding muscles in Aplysia

Abstract

The extrinsic buccal muscles in Aplysia are responsible for the overall protraction and retraction of the buccal mass during feeding. The six pairs of extrinsic muscles are organized into two groups, consisting of three protractors and three retractors. Insights into how the extrinsic muscles are controlled were obtained by examining the organization of the motor neurons that innervated them. The extrinsic buccal muscles are innervated by cerebral ganglion nerves and neurons. All the muscles examined appear to be multiply innervated. Identified neurons in the cerebral B, E, and G clusters were found to be motor neurons for individual extrinsic muscles. Some extrinsic muscles had both excitatory and inhibitory innervation. Two synergistic muscles, the extrinsic ventrolateral protractor (ExVLP) and the extrinsic dorsal protractor (ExDP), had common excitatory innervation by identified neuron E5. Two antagonistic muscles, the ExVLP and the extrinsic ventral retractor (ExVR), also had common innervation. Identified neuron E1 appeared to be an inhibitory motor neuron for the ExVLP but an excitatory motor neuron for the ExVR. Common innervation provides a simple mechanism for coordinating synergistic and antagonistic extrinsic muscles. On the basis of these data, a model for the control of buccal mass protraction and retraction is proposed. Bursting by extrinsic buccal muscles was coordinated with cyclic activity in the intrinsic muscles of the buccal mass. Antagonistic extrinsic muscles burst antiphasically and synergistic extrinsic muscles burst in phase when the buccal mass was fully protracted and exhibited a series of rhythmic contractions. Additionally, cerebral E cluster neurons burst in phase with stereotyped rhythmic buccal motor neuron discharges recorded from buccal nerves. The cerebral E cluster motor neurons were coordinated by common synaptic input. No monosynaptic connections were observed; homologous neurons in each E cluster received synaptic input with similar but not identical timing, indicating that the interneurons that coordinate the homologous motor neurons are synchronized. The source of the rhythm that drives synaptically mediated cerebral extrinsic muscle motor neuron bursting was in the buccal ganglia. Cutting one cerebral-buccal connective eliminated E neuron bursting on that side but had no effect on homologous neurons on the intact side. This suggests that a single oscillator in the buccal ganglia may coordinate both the extrinsic and intrinsic buccal muscles during feeding.