Functional Recovery after Lesion of a Central Pattern Generator

Abstract

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.

Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry

“…After hemisection, sprouting of sensory afferents has been reported on the lesion side (Helgren and Goldberger 1993;Murray and Goldberger 1974), and several segmental reflexes have been shown to become asymmetric Malmsten 1983a, 1983b;Malmsten 1983;Muir et al 1998). Changes within the functional connectivity of the CPG following a lesion within the intrinsic circuitry have also been reported in mollusks, explaining recovery of escape behavior without the need for regeneration (Sakurai and Katz 2009). In addition, and in accordance with our results, several studies have previously shown asymmetric changes imprinted in the spinal circuitry that were revealed by a complete SCI Rossignol 2003a, 2003b;Frigon and Rossignol 2008;).…”

Effect of Locomotor Training in Completely Spinalized Cats Previously Submitted to a Spinal Hemisection

“…The fast reversion of left/right asymmetries observed in trained cats suggests that changes have occurred in the functional connectivity of the central pattern generators (CPG) controlling left and right HLs. An elegant work in an invertebrate CPG also shows that a new balance between left and right sides can be established following a lesion of the swim CPG (Sakurai and Katz, 2009). The fast recovery of escape behavior was shown to result from changes in synaptic weighting rather than anatomical reorganization.…”

Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry

“…The adaptations observed after hemisection appeared to be mainly maintained by remaining descending pathways, thus creating a new left/right balance within the spinal circuits. In addition, physiological changes in synaptic weighting can occur within the CPG itself and could account for the establishment of a new balance between left and right sides (Sakurai and Katz 2009). Investigations are in progress to study the impact of locomotor training during the same base period.…”