Competitive elimination of foreign motor innervation on autonomic neurones in the frog heart.
1. Somatic motoneurones are capable of forming functional synapses when redirected to vagotomized autonomic neurones in the frog heart. We tested if regenerating vagus nerves could reinnervate ganglion cells in the presence of foreign hypoglossal innervation and, furthermore, whether hypoglossal innervation persisted when vagal axons regenerated to the heart. 2. Simulating the redirected hypoglossus nerve produced a parasympathetic-like cardiac inhibition in the absence of vagal regeneration. However, when the vagus nerve was allowed to regenerate to the heart, vagal cardio-inhibition was restored and hypoglossal inhibition disappeared. 3. Intracellular recordings showed that 71% of the cardiac ganglion cells were innervated by hypoglossal axons before vagal regeneration, but that this value fell to less than 9% over a period of 40 weeks during vagal regeneration. 4. If the vagus nerve was prevented from regenerating to the heart, hypoglossal innervation did not decline, indicating that elimination of the foreign motor innervation was dependent upon vagal reinnervation. 5. Although hypoglossal terminals formed synapses only on the axons of parasympathetic ganglion cells, regenerating vagal fibres re-established synaptic contact both on axons as well as on neuronal perikarya. 6. The data indicate that in the frog parasympathetic cardiac ganglion, extensive synaptic remodelling can take place during reinnervation and that previously established, inappropriate inputs can be functionally eliminated by regeneration of the native nerve supply.
D000818:Animals; D005726:Ganglia, Parasympathetic / Q000502:physiology* / Q000648:ultrastructure; D006321:Heart / Q000294:innervation; D006339:Heart Rate; D007002:Hypoglossal Nerve / Q000502:physiology; D009046:Motor Neurons / Q000502:physiology*; D009416:Nerve Regeneration; D011894:Rana pipiens; D013569:Synapses / Q000502:physiology / Q000648:ultrastructure; D014630:Vagus Nerve / Q000502:physiology