Comparative analysis of hyperexcitability and synaptic facilitation induced by nerve injury in two populations of mechanosensory neurones of Aplysia californica.

Long-term effects of nerve injury on electrophysiological properties were compared in two populations of mechanosensory neurones in Aplysia californica: the J and K clusters in the cerebral ganglia and the VC clusters in the pleural ganglia. Following crush of cerebral nerves containing their axons, the cerebral J/K sensory neurones showed long-term changes that were quite similar to alterations previously described in the VC sensory neurones after either axonal injury or aversive learning. These changes include synaptic facilitation, an increase in soma excitability and spike duration, and a decrease in spike threshold and afterhyperpolarization. In addition, simultaneous crush of both the cerebral and pedal nerves in the same animals produced alterations in the cerebral J/K sensory neurones and pleural VC sensory neurones that were virtually identical. The incidence of hyperexcitability was the same in cerebral J/K and pleural VC sensory neurones when all their axons were crushed, even though the former population includes many neurones that probably have appetitive functions while the latter population appears to be made up exclusively of neurones with defensive functions. Long-term plasticity in both sensory populations failed to occur when nerves lacking axons of the tested neurones were crushed, even when the crush site was very close to the somata of the sensory neurones. This axonal specificity argues against a role for delayed activation of facilitatory interneurones in triggering the plasticity. Several observations are consistent with a triggering role for either (1) intracellular signals released directly by axonal injury or (2) extracellular signals released locally by other axons or injured support cells, or by immunocytes attracted to the injured site.