Peripheral nerve pathways to neurons in the guinea pig inferior mesenteric ganglion determined electrophysiologically after chronic nerve section

Abstract

Peripheral synaptic pathways to neurons in the guinea pig inferior mesenteric ganglion (IMG) were studied. Nerve trunks innervating neurons in the ganglion were surgically sectioned and intracellular electrical responses to nerve stimulation were measured 6–8 days after surgery. In all animals ganglia were decentralized by removal of the lumbar sympathetic chain ganglia L 2 through L 4 and in addition two peripheral nerves were sectioned leaving the ganglion innervated by only one peripheral nerve. Fast and slow excitatory postsynaptic potentials (EPSPs) were evoked with electrical stimulation of each of the nerve trunks and with distension of the colon. The thresholds to evoke fast EPSPs and the amplitude of slow EPSPs were compared for each nerve trunk among the different surgical groups including sham-operated controls and completely denervated ganglia. Both fast and slow EPSPs could be evoked electrically from each intact peripheral nerve trunk after the other three nerve trunks had been sectioned, which demonstrates that nerve fibers with cell bodies in the regions innervated by the peripheral nerves make functional synaptic connections with neurons in the inferior mesenteric ganglion. In general, nerve sections increased the threshold for evoking fast EPSPs and decreased the amplitude of electrically-evoked slow EPSPs compared to control ganglia. Synaptic potentials could also be evoked with stimulation of cut nerve trunks, demonstrating that branches of nerve fibers from peripheral nerves enter other nerve trunks. The hypogastric nerve was unique in that branches of axons eliciting fast but not slow synaptic potentials in the ganglion entered this nerve trunk. Distension-induced fast and slow EPSPs were present only if the lumbar colonic nerve was intact and they were not altered by section of the other nerve trunks. In contrast, the slow EPSPs evoked with electrical stimulation of the lumbar colonic nerve were significantly smaller when at least one other nerve trunk was sectioned suggesting that the axon branches from other nerve trunks which enter the lumbar colonic nerve are not activated by distension. These studies demonstrate that neurons eliciting either fast or slow synaptic potentials with cell bodies in regions innervated by the peripheral nerve trunks make functional synaptic connections with neurons of the inferior mesenteric ganglion. The results also suggest that the majority of mechanosensory neurons mediating excitatory synaptic responses to colon distension are neurons with a peripheral cell body.