Correlation of electrophysiological and morphological characteristics of enteric neurons in the mouse colon

Abstract

We report on the first correlative study of the electrophysiological properties, shapes, and projections of enteric neurons in the mouse. Neurons in the myenteric plexus of the mouse colon were impaled with microelectrodes containing biocytin, their passive and active electrophysiological properties determined, and their responses to activation of synaptic inputs investigated. Biocytin, injected into the neurons from which recordings were made, was converted to an optically dense product and used to determine the shapes of neurons. By electrophysiological properties, almost all neurons belonged to one of two classes, AH neurons or S neurons. AH neurons had a biphasic repolarization of the action potential, and slow afterhyperpolarizing potentials usually followed the action potentials. S neurons had monophasic repolarizations, no slow afterhyperpolarization, and fast excitatory postsynaptic potentials in response to fibre tract stimulation. By shape, neurons were divided into Dogiel type II (28/136 neurons) and uniaxonal neurons. Dogiel type II neurons had large, smooth-surfaced cell bodies and several long processes that supplied branches within myenteric ganglia. All Dogiel type II neurons had AH electrophysiology; conversely, most AH neurons had Dogiel type II morphology. The majority of uniaxonal neurons had lamellar dendrites, i.e., Dogiel type I morphology. They projected to the circular muscle (circular muscle motor neurons), to the longitudinal muscle (longitudinal muscle motor neurons), and to other myenteric ganglia (interneurons) and in some cases could not be traced to target cells. All S neurons were uniaxonal. A small proportion of uniaxonal neurons (3/70) had AH electrophysiology. Fast excitatory synaptic potentials were only recorded from uniaxonal neurons and were in most cases blocked by nicotinic receptor antagonists. A small component of fast excitatory transmission in some neurons was antagonized by the purine receptor antagonist PPADS. Slow excitatory postsynaptic potentials were observed in both AH and S neurons. Slow inhibitory postsynaptic potentials were recorded from S neurons. We conclude that the major classes of neurons are Dogiel type II neurons with AH electrophysiological properties and Dogiel type I neurons with S electrophysiological properties. The S/Dogiel type I neurons include circular muscle motor neurons, longitudinal muscle motor neurons, and interneurons.

Transplanted progenitors generate functional enteric neurons in the postnatal colon

“…The durations and amplitudes of evoked fEPSPs and the number of fEPSPs in groups elicited by single-pulse stimulations were also reduced by hexamethonium (data not shown). The resting membrane potential and input resistance of graft-derived neurons (Table 1) were similar to those recently reported for P0 and P10 enteric neurons (52), but the neurons were more depolarized than adult enteric neurons (53).…”

“…S neurons are uniaxonal and show monophasic repolarization after an AP and fEPSPs in response to fiber tract stimulation. In contrast, AH neurons show a biphasic repolarization and a slow afterhyperpolarizing potential after an AP and rarely display fEPSPs (53). In the current study, only a single electrophysiological class of neuron was observed, possessing properties very similar to S neurons (53), in the mouse distal colon.…”

“…In contrast, AH neurons show a biphasic repolarization and a slow afterhyperpolarizing potential after an AP and rarely display fEPSPs (53). In the current study, only a single electrophysiological class of neuron was observed, possessing properties very similar to S neurons (53), in the mouse distal colon. Although AH neurons account for about 20% of neurons in the mouse distal colon (53), we did not encounter graftderived neurons with AH-type electrophysiology.…”

“…Importantly, the presence of fEPSPs showed that the graft-derived neurons had integrated into the neuronal circuitry, although we were unable to determine whether the synaptic inputs arose from other graftderived neurons, from the recipient's neurons, or both. There are 2 main electrophysiological classes of myenteric neurons in the ENS, S neurons and AH neurons (53,69). S neurons are uniaxonal and show monophasic repolarization after an AP and fEPSPs in response to fiber tract stimulation.…”

Cholinergic giant migrating contractions in conscious mouse colon assessed by using a novel noninvasive solid-state manometry method: modulation by stressors

“…However, the type, pattern, frequency, magnitude, and regulation of colonic motor activity in conscious mice are still not known. This contrasts with the vast knowledge of mouse colonic enteric neuron physiology (16,44,45,53) and the availability of large and growing number of genetically modified mice with great potential as tools to help understand colonic motility and its impacts in health and disease states.…”