Intracellular recordings from cells in the myenteric plexus of the rat duodenum (original) (raw)
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The Journal of physiology, 1989
1. Intracellular recording methods were used to investigate the cellular neurophysiology of ganglion cells in the myenteric plexus of the guinea-pig rectum. The rectum is a region of the gastrointestinal tract with specialized functions that include reflex relaxation of the internal and sphincter during defaecation. Electrical and synaptic properties of myenteric neurones in the rectum had not previously been studied. Therefore, the overall aim of the work was to describe electrical and synaptic behaviour and identify neurophysiological properties of rectal neurones that might be related to specialization of function in this region of the gut. 2. Thirty-four (58%) of fifty-nine impaled cells had electrophysiological properties of AH/type 2 enteric neurones. Eighteen (30%) behaved like type 3 neurones and only two (3%) behaved like S/type 1 enteric neurones. Three per cent were presumably glial cells and the remainder were unclassifiable. 3. Nicotinic cholinergic fast EPSPs were reco...
Neuroscience, 1997
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, smoothsurfaced 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.
Synaptic behaviour in the myenteric plexus of the guinea-pig gastric antrum
The Journal of physiology, 1992
1. Intracellular recording methods were used to study the synaptic behaviour of neurones in the myenteric plexus of the guinea-pig gastric antrum. Synaptic potentials occurred spontaneously or were evoked by focal electrical stimulation of interganglionic fibre tracts. Synaptic events consisted of fast and slow excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs). 2. Fast EPSPs with durations less than 20 ms were evoked in every antral neurone in a population sample of 370 cells. Most of the ganglion cells received multiple inputs from axons entering the individual ganglia in several different interganglionic fibre tracts. Many of the neurones also received input from multiple axons projecting in individual fibre tracts. The fast EPSPs behaved like nicotinic cholinergic EPSPs. They were evoked at stimulus frequencies up to 60 Hz without evidence of the run-down characteristic of fast EPSPs in the intestine. 3. Slow EPSPs were evoked by repetitive...
1999
Intracellular recordings were made from myenteric neurons of the guinea-pig distal colon to determine their electrical behaviour in response to intracellular current injection and stimulation of synaptic inputs. The recording microelectrode contained the intracellular marker biocytin, which was injected into impaled neurons so that electrophysiology, shape and immunohistochemistry could be correlated. Myenteric neurons in the distal colon were divided into four morphological groups based on their shapes and projections. One Ž . group 29 of the 78 that were characterized electrophysiologically, morphologically and immunohistochemically was the multiaxonal Ž . Dogiel type II neurons, the majority 25r29 of which were calbindin immunoreactive. Each of these neurons had an inflection on the Ž . falling phase of the action potential that, in 24r29 neurons, was followed by a late afterhyperpolarizing potential AHP . Slow excitatory postsynaptic potentials were recorded in 20 of 29 Dogiel type II neurons in response to high frequency internodal strand stimulation and two neurons responded with slow inhibitory postsynaptic potentials. Low amplitude fast excitatory postsynaptic potentials occurred in 3 of 29 Dogiel type II neurons. Neurons of the other three groups were all uniaxonal: neurons with Dogiel type I morphology, filamentous ascending interneurons and small filamentous neurons with local projections to the longitudinal or circular muscle or to the tertiary plexus. Dogiel type I neurons were often immunoreactive for nitric oxide synthase or calretinin, as were some small filamentous neurons, while all filamentous ascending interneurons tested were calretinin immunoreactive. All uniaxonal neurons exhibited prominent fast excitatory postsynaptic potentials and did not have a late AHP following a single action potential, that is, all uniaxonal neurons displayed S type electrophysiological characteristics. However, in 6r19 Dogiel type I neurons and 2r8 filamentous ascending interneurons, a prolonged hyperpolarizing potential ensued when more than one action potential was evoked. Slow depolarizing postsynaptic potentials were observed in 20r29 Dogiel type I neurons, 6r8 filamentous ascending interneurons and 8r12 small filamentous neurons. Six of 29 Dogiel type I neurons displayed slow inhibitory postsynaptic potentials, as did 2r8 filamentous ascending interneurons and 4r12 small filamentous neurons. These results indicate that myenteric neurons in the distal colon of the guinea-pig are electrophysiologically similar to myenteric neurons in the ileum, duodenum and proximal colon. Also, the correlation of AH electrophysiological characteristics with Dogiel type II morphology and S electrophysiological characteristics with uniaxonal morphology is preserved in this region. However, filamentous ascending interneurons have not been encountered in other regions of the gastrointestinal tract and there are differences between the synaptic properties of neurons in this region compared to other regions studied, including the presence of slow depolarizing postsynaptic potentials that appear to involve conductance increases and frequent slow inhibitory postsynaptic potentials. q 1999 Published by Elsevier Science B.V. All rights reserved.
Synaptic transmission from the submucosal plexus to the myenteric plexus in Guinea-pig ileum
Neurogastroenterology & Motility, 2008
Stimulation of the myenteric plexus results in activation of submucosal neurons and dilation of arterioles, one way that motility and secretion can be coupled together. The present study aimed to examine the converse, whether myenteric neurons receive synaptic input from the submucosal plexus (SMP). Intracellular recordings were made from guinea-pig ileal myenteric neurons while the SMP was electrically stimulated. Of the 29 neurons studied (13 S and 16 AH neurons), stimulation of the SMP evoked a synaptic potential in only seven cells, or 24% of neurons. When the SMP was situated oral to the myenteric plexus, 4 of 13 (31%) myenteric neurons had synaptic input. When it was situated circumferential, 2 of 8 (25%) had input, and when the SMP was situated anal 1 of 8 (13%) had input. Overall, 5 of the 13 (38%) S neurons responded with fast excitatory post-synaptic potentials (EPSPs), one of which also showed a slow EPSP, while 2 of the 16 (13%) AH neurons responded with a slow EPSP. This study indicates that the synaptic input from the SMP to myenteric neurons is relatively sparse. Whether this input is less important than the myenteric to submucosal input or simply represents a more selective form of control is unknown.
Intracellular recordings from myenteric neurones in the human colon
The Journal of physiology, 1987
1. Intracellular recordings were made from cells in the myenteric plexus of the human colon in freshly dissected tissue obtained from patients undergoing surgery for the removal of carcinomas or diverticular bowel. 2. Twenty-seven cells from ten preparations were classified as neurones and had overshooting action potentials, an average resting potential of -54 +/- 9 mV, an average input impedance of 1.05 +/- 0.59 x 10(8) omega and a variety of synaptic inputs. 3. Twenty-three (out of twenty-five neurones tested) received nicotinic fast excitatory synaptic inputs (fast e.p.s.p.s) that were blocked reversibly by hexamethonium and mimicked by acetylcholine. These nerve cells bore a close resemblance to S cells that have been characterized in the guinea-pig small-bowel myenteric plexus. 4. One cell had a long after-hyperpolarization following its impulses and was similar to AH cells in the guinea-pig small bowel. 5. Three neurones received inhibitory synaptic inputs, up to 15 mV in ampl...
Excitatory synaptic inputs on myenteric Dogiel type II neurones of the pig ileum
The Journal of Comparative Neurology, 2001
The synaptic input on myenteric Dogiel type II neurones (n ϭ 63) obtained from the ileum of 17 pigs was studied by intracellular recording. In 77% of the neurones, electrical stimulation of a fibre tract evoked fast excitatory postsynaptic potentials (fEPSPs) with an amplitude of 6 Ϯ 5 mV (mean Ϯ S.D.) and lasting 49 Ϯ 29 ms. The nicotinic nature of the fEPSPs was demonstrated by superfusing hexamethonium (20 M). High-frequency stimulation (up to 20 Hz, 3 seconds) did not result in a rundown of the fEPSPs, and did not evoke slow excitatory or inhibitory postsynaptic potentials. The effects of neurotransmitters, possibly involved in these excitatory responses, were investigated. Pressure microejection of acetylcholine (10 mM in pipette) resulted in a fast nicotinic depolarisation in 67%(18/27) of the neurones (13 Ϯ 9 mV, duration 7.0 Ϯ 7.2 seconds) as did 1,1-dimethyl-4phenylpiperazinium iodide (DMPP) application (10 mM; 14 Ϯ 10 mV, duration 4.1 Ϯ 2.8 seconds) in 76%of the cells. The fast nicotinic response to acetylcholine was sometimes (6/27) followed by a slow muscarinic depolarisation (8 Ϯ 4 mV; duration 38.7 Ϯ 10.8 seconds). Immunostaining revealed 5-hydroxytryptamine hydrochloride (5-HT)-and calcitonin generelated peptide (CGRP)-positive neuronal baskets distributed around and in close vicinity to Dogiel type II neuronal cell bodies. Microejection of 5-HT (10 mM) resulted in a fast nicotiniclike depolarisation (12 Ϯ 6 mV, duration 3.0 Ϯ 1.3 seconds) in 4 of 8 neurones tested, whereas microejection of CGRP (20 mM) gave rise to a slow muscarinic-like depolarisation (6 Ϯ 2 mV, duration 56.0 Ϯ 27.5 seconds) in 8 of 12 neurones tested. In conclusion, myenteric Dogiel type II neurones in the porcine ileum receive diverse synaptic input. Mainly with regard to the prominent presence of nicotinic responses, these neurones behave contrary to their guinea pig counterparts. J. Comp. Neurol. 432:137-154, 2001.
Neurochemical classification of myenteric neurons in the guinea-pig ileum
Neuroscience, 1996
A strategy has been developed to identify and quantify the different neurochemical populations of myenteric neurons in the guinea-pig ileum using double-labelling fluorescence immunohistochemistry of whole-mount preparations. First, six histochemical markers were used to identify exclusive, nonoverlapping populations of nerve cell bodies. They included immunoreactivity for the calcium binding proteins calbindin and calretinin, the neuropeptides vasoactive intestinal polypeptide, substance P and somatostatin, and the amine, S-hydroxytryptamine. The sizes of these populations of neurons were established directly or indirectly in double-labelling experiments using a marker for all nerve cell bodies. Each of these exclusive populations was further subdivided into classes by other markers, including immunoreactivity for enkephalins and neurofilament protein triplet. The size of each class was then established directly or by calculation. These distinct, neurochemically-identified classes were related to other published work on the histochemistry, electrophysiology and retrograde labelling of enteric neurons and to the simple Dogiel morphological classification.
Neuroscience, 1998
Nerve circuits within the proximal duodenum were investigated using a combination of immunohistochemistry for individual neuron markers and lesion of intrinsic nerve pathways to determine axon projections. Cell shapes and axonal projections were also studied in cells that had been injected with a marker substance. Several major neuron populations were identified. Calbindin immunoreactivity occurred in a population of myenteric nerve cells with Dogiel type II morphology. These had axons that projected to other myenteric ganglia, to the circular muscle and to the mucosa. All were immunoreactive for the synthesizing enzyme for acetylcholine, choline acetyltransferase, and some were also immunoreactive for calretinin. Myenteric neurons with nitric oxide synthase immunoreactivity projected anally to the circular muscle. These were also immunoreactive for vasoactive intestinal peptide, and proportions of them had enkephalin and/or neuropeptide Y immunoreactivity. It is suggested that they are inhibitory motor neurons to the circular muscle. A very few (about 2%) of nitric oxide synthase-immunoreactive neurons had choline acetyltransferase immunoreactivity. Tachykinin (substance P)-immunoreactive nerve cells were numerous in the myenteric plexus. Some of these projected orally to the circular muscle and are concluded to be excitatory motor neurons. Others projected to the tertiary plexus which innervates the longitudinal muscle and others provided terminals in the myenteric plexus. Two groups of descending interneurons were identified, one with somatostatin immunoreactivity and one with vasoactive intestinal peptide immunoreactivity. The two most common nerve cells in submucous ganglia were neuropeptide Yand vasoactive intestinal peptide-immunoreactive nerve cells. Both provided innervation of the mucosa. There was also a population of calretinin-immunoreactive submucous neurons that innervated the mucosal glands, but not the villi.
The Anatomical record, 1989
Recent electrophysiological studies of neurons of the myenteric plexus of the corpus of the guinea pig stomach have revealed that slow synaptic events are extremely rare. In contrast, they are commonly encountered in similar investigations of myenteric ganglia of the guinea pig small intestine. The current immunocytochemical analysis of the myenteric plexus and innervation of the muscularis externa of the corpus of the guinea pig stomach was undertaken in order to determine whether putative neurotransmitters capable of mediating slow synaptic events are present in gastric ganglia. A major difference between the small intestine and the stomach was found in the innervation of the musculature. Whereas the longitudinal muscle layer of the small intestine contains very few nerve fibers and is innervated mainly at its interface with the myenteric plexus, the longitudinal muscle of the corpus of the stomach contained as many varicose substance P (SP)-, vasocative intestinal polypeptide (VI...