Regulation of intraganglionic synapses among rabbit parasympathetic neurones.

1. The response of parasympathetic neurones to the removal of preganglionic innervation was studied in the ciliary ganglia of adult rabbits. After section of the preganglionic oculomotor nerve, individual ciliary neurones were characterized electrophysiologically by intracellular recording, and morphologically by intracellular injection of horseradish peroxidase. 2. Within the first 24-48 h after nerve section, only two of fifty-nine neurones responded to antidromic stimulation of the postganglionic ciliary nerve with synaptic potentials. This result indicates that synaptic connections between principal neurones are rare in normal ganglia. 3. One week after denervation, however, excitatory postsynaptic potentials were recorded in thirty-nine out of fifty-three cells examined. Thus there is a rapid and extensive formation of intraganglionic connections after denervation. Morphological analysis of these ganglion cells showed numerous fine processes arising from the cell bodies and dendrites; such neurites were not present among control neurones. Many of these newly formed processes appeared to form synapses on neighbouring cells. 4. A similar proportion of neurones (about two-thirds of the cells) showed antidromically evoked excitatory postsynaptic potentials 2 weeks after denervation. Dendrites were still longer and more complex than controls at this time. After several months the morphology and prevalence of intraganglionic connections returned to normal as the ganglion became reinnervated. 5. Thus, denervation of rabbit ciliary ganglion cells induces the rapid formation of large numbers of functional synaptic connections among ganglion cells. It is postulated that local regulatory factors govern connections between parasympathetic ganglion cells. After denervation, these trophic signals are no longer modulated by presynaptic axons and they exert a stimulus for sprouting and synapse formation among this population of cholinergic neurones.