Functional Recovery after Lesion of a Central Pattern Generator

In cases of neuronal injury when regeneration is restricted, functional recovery can occur through reorganization of the remaining neural circuitry. We found an example of such recovery in the central pattern generator (CPG) for the escape swim of the mollusc Tritonia diomedea. The CPG neurons are bilaterally represented and each neuron projects an axon through one of two pedal commissures. Cutting the posterior pedal commissure [pedal nerve 6 (PdN6)] in the animal or in the isolated brain caused a deficit in the swim behavior and in the fictive motor pattern, respectively, each of which recovered over the course of 20 h. Locally blocking spiking activity in PdN6 with sodium-free saline and/or tetrodotoxin disrupted the motor pattern in a reversible manner. Maintained blockade of PdN6 led to a functional recovery of the swim motor pattern similar to that observed in response to cutting the commissure. Among the CPG neurons, cerebral neuron 2 (C2) makes functional connection onto the ventral swim interneuron-B (VSI) in both pedal ganglia. Cutting or blocking PdN6 eliminated C2-evoked excitation of VSI in the pedal ganglion distal to the lesion. Associated with the recovery of the swim motor pattern, the synaptic action of C2 onto VSI in the proximal pedal ganglion changed from being predominantly inhibitory to being predominantly excitatory. These results show that the Tritonia swim CPG undergoes adaptive plasticity in response to the loss of critical synaptic connections; reversal of synaptic action in the CPG may be at least partially responsible for this functional recovery.