Electrophysiological features of morphological Dogiel type II neurons in the myenteric plexus of pig small intestine.

Abstract

By intracellular recording, 99 myenteric neurons with Dogiel type II morphology were electrophysiologically characterized in the porcine ileum and further subdivided into three groups based on their different types of afterhyperpolarization (AHP). In response to a depolarizing current injection, a fast AHP (fAHP; duration 34 +/- 11 ms; amplitude -11 +/- 6 mV; mean +/- SD) immediately followed every action potential in all neurons. In 32% of the neurons, this fAHP was the sole type of hyperpolarization recorded. Statistical analysis revealed the presence of two neuronal subpopulations that displayed either a long-lasting medium AHP (mAHP; duration after a single spike 773 +/- 753 ms; 51% of neurons) or a slow AHP (sAHP; 4, 205 +/- 1,483 ms; 17%). Slow AHP neurons also differed from mAHP neurons in the delayed onset of the AHP (mAHP 0 ms; sAHP 100-200 ms), as well as in maximum amplitude values and in the time to reach this amplitude (t(max); 148 +/- 11 ms vs. 628 +/- 108 ms). Medium AHP neurons further differed from the sAHP neurons in the occurrence of the AHP following subthreshold current injection and in their resting membrane potential (mAHP, -53 +/- 8 mV; sAHP, -62 +/- 10 mV). Medium AHP and sAHP behaved similarly in that a higher number of spikes increased their amplitude and duration, but not t(max). The majority of neurons fired multiple spikes (up to 25) in response to a 500-ms current injection (81/99) and showed a clear TTX-resistant shoulder on the repolarizing phase of the action potential (77/99), irrespective of the presence of sAHP or mAHP. These results demonstrate that the porcine Dogiel type II neurons differ in various essential electrophysiological properties from their morphological counterparts in the guinea pig ileal myenteric plexus. The most striking interspecies differences were the low occurrence of sAHP (17% vs. 80-90% in guinea pig) with relatively small amplitude (-5 vs. -20 mV), the high occurrence of mAHPs (unusual in guinea pig) and the ability to fire long spike trains (up to 25 spikes vs. 1-3 in guinea pig). In fact, Dogiel type II neurons in porcine ileum combine distinct electrophysiological features considered typical of either S-type or sAHP-type neurons in guinea pig. It can therefore be concluded that in spite of a similar morphology, Dogiel type II neurons do not behave electrophysiologically in a universal way in large and small mammals.