Contralateral sprouting and compensatory innervation following the permanent lesion of a ganglionic connective in the snail

Abstract

The fate of sprouted fibres was examined following long-term recovery from lesions to the central nervous system of the snail Achatina fulica. Axonal dye-labelling of one of the cerebrobuccal connectives (CBC), following either a cut or a crush to the opposite CBC, revealed supernumerary labelling of neuronal elements in both the cerebral and buccal ganglia in the weeks following treatment. A part of this sprouting response involved the rerouting of axonal projections from injured neurones that project contralaterally into the uninjured CBC. In addition, intracellular dye-fills, immunocytochemistry for detection of serotonin and electrophysiological measurements all revealed that a contralateral, uninjured neurone, the metacerebral giant (MCG) cell, sprouted new processes to invade the buccal ganglion denervated by the lesion. The contralateral MCG also increased synaptic drive over a neurone in the denervated buccal ganglion, a cell that normally receives strong input only from the lesioned ipsilateral MCG. After 5 weeks of recovery, morphological and electrophysiological measurements returned to normal levels in animals receiving a crush to the CBC, suggesting a retraction of sprouted projections following successful regeneration across the lesioned pathway. In contrast, the measurements indicative of sprouted fibres continued for up to 5 months when the regenerative response was prevented by cutting the CBC. Together, these results suggest that both the cessation of sprouting and the eventual retraction of sprouted fibres in Achatina fulica is contingent upon successful regeneration of the damaged axonal pathway.