Electrophysiological characteristics distinguish three classes of neuron in submucosal ganglia of the guinea-pig distal colon

Abstract

Intracellular recordings were made from neurons in the submucosal ganglia of the guinea-pig distal colon. The recording electrode contained the intracellular marker biocytin, which was injected into neurons so that their electrophysiological characteristics could be correlated with their shape. Correlations of electrophysiology and shape have not been reported previously for neurons in this region. Three types of neuron were identified on electrophysiological grounds. Neurons of the first type (S neurons) had tetrodotoxin-sensitive soma action potentials, and received fast and slow excitatory synaptic inputs. They had uniaxonal morphologies and may function as secretomotor or possibly vasomotor neurons. The second type (AH neurons) received only slow synaptic input, while the soma action potential had tetrodotoxin-sensitive and -insensitive components with a shoulder on the falling phase and a long-lasting afterhyperpolarisation of the membrane potential following a single action potential. Neurons of this type had multipolar morphologies and provided dense innervation of adjacent submucosal ganglia. These neurons are similar to the submucosal intrinsic primary afferent neurons of the guinea-pig small intestine. The final type of neuron [the low-threshold (LT) neuron] had electrophysiological characteristics that set it apart from those described previously within enteric plexuses. They expressed tetrodotoxin-insensitive voltage-gated soma currents, did not have long-lasting afterhyperpolarisations and received only slow synaptic input. In addition, these neurons were very excitable: they had large input resistances and low thresholds for action potential discharge, and often fired action potentials in the absence of stimulation. Neurons with these characteristics were uniaxonal and thus are likely to be secretomotor or possibly vasomotor neurons.

This study has shown that submucosal neurons of the distal colon fall into three distinct types, which can be distinguished by a combination of electrophysiological and morphological criteria.