Influence of the mucosa on the excitability of myenteric neurons (original) (raw)
Related papers
American Journal of Physiology-Gastrointestinal and Liver Physiology, 1997
Responses of myenteric AH and S neurons to local application of chemicals to the mucosa of the guinea pig small intestine were obtained using conventional intracellular recording techniques. Preparations were dissected to reveal the myenteric plexus over one-half of the circumference of the gut with intact mucosa on the the half. Neurons were impaled within the exposed one-half, whereas potential stimulants, in buffered saline, were transiently applied to the mucosa, 1-1.5 mm circumferential from the impalement. The stimulants elicited action potentials (AP) in AH neurons that did not arise from synaptic activity. AH neurons also responded with slow excitatory postsynaptic potentials (EPSP). S neurons were activated synaptically, via fast and slow EPSP, but not nonsynaptically. Mucosal application of solutions of a low pH (3-5) or a high pH (9-11) were both effective stimulants. Solutions of a neutral pH, which was also a control for mild mechanical stimulation, were usually ineffec...
Characteristics of mucosally projecting myenteric neurones
1999
The NK_3 receptor antagonist SR 142801 (1 ìÒ) significantly decreased the amplitude and duration of the sEPSPs; the NK_1 receptor antagonist CP-99,994 (1 ìÒ) was ineffective. Atropine (0•5 ìÒ) increased the duration but not the amplitude of the sEPSPs. 5. Microejection of 100 mÒ sodium butyrate onto the neurones induced in 90% of the DiIlabelled neurones a transient depolarization associated with an increased excitability. In neurones with SHPs sodium butyrate evoked, additionally, a late onset hyperpolarization. Perfusion of 0•1-10 mÒ sodium butyrate induced a dose-dependent increase in neuronal excitability. Sodium butyrate was ineffective when applied directly onto the mucosa. 6. Mucosally projecting myenteric neurones of the colon are multipolar AH neurones with NK_3-mediated slow EPSPs and somal butyrate sensitivity.
Characterization of Myenteric Sensory Neurons in the Mouse Small Intestine
Journal of Neurophysiology, 2006
Characterization of myenteric sensory neurons in the mouse small intestine. . We recorded from myenteric AH/Dogiel type II cells, demonstrated mechanosensitive responses, and characterized their basic properties. Recordings were obtained using the mouse longitudinal muscle myenteric plexus preparation with patch-clamp and sharp intracellular electrodes. The neurons had an action potential hump and a slow afterhyperpolarization (AHP) current. The slow AHP was carried by intermediate conductance Ca 2ϩ -dependent K ϩ -channel currents sensitive to charybdotoxin and clotrimazole. All possessed a hyperpolarization-activated current that was blocked by extracellular cesium. They also expressed a TTX-resistant Na ϩ current with an onset near the resting potential. Pressing on the ganglion containing the patched neuron evoked depolarizing potentials in 17/18 cells. The potentials persisted after synaptic transmission was blocked. Volleys of presynaptic electrical stimuli evoked slow excitatory postsynaptic potentials (EPSPs) in 9/11 sensory neurons, but 0/29 cells received fast EPSP input. The slow EPSP was generated by removal of a voltageinsensitive K ϩ current. Patch-clamp recording with a KMeSO 4containing, but not a conventional KCl-rich, intracellular solution reproduced the single-spike slow AHPs and low input resistances seen with sharp intracellular recording. Cell-attached recording of intermediate conductance potassium channels supported the conclusion that the single-spike slow AHP is an intrinsic property of intestinal AH/sensory neurons. Unitary current recordings also suggested that the slow AHP current probably does not contribute significantly to the high resting background conductance seen in these cells. The characterization of mouse myenteric sensory neurons opens the way for the study of their roles in normal and pathological physiology. Downloaded from Bers DM, Patton CW, and Nuccitelli R. A practical guide to the preparation of Ca 2ϩ buffers. Methods Cell Biol 40: 3-29, 1994. Bertrand PP and Galligan JJ. Signal-transduction pathways causing slow synaptic excitation in guinea pig myenteric AH neurons. Am J Physiol Gastrointest Liver Physiol 269: G710 -G720, 1995. Bertrand PP, Kunze WA, Bornstein JC, Furness JB, and Smith ML. Analysis of the responses of myenteric neurons in the small intestine to chemical stimulation of the mucosa. Am J Physiol Gastrointest Liver Physiol 273: G422-G435, 1997. Bertrand PP and Thomas EA. Multiple levels of sensory integration in the intrinsic sensory neurons of the enteric nervous system. Clin Exp Pharmacol Physiol 31: 745-755, 2004. Bian X, Ren J, DeVries M, Schnegelsberg B, Cockayne DA, Ford AP, and Galligan JJ. Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. J Physiol 551: 309 -322, 2003. Bornstein JC, Furness JB, and Kunze WA. Electrophysiological characterization of myenteric neurons: how do classification schemes relate? J Auton Nerv
The Journal of Comparative Neurology, 2004
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.
the Mouse Small Intestine Characterization of Myenteric Sensory Neurons in
2015
We recorded from myenteric AH/Dogiel type II cells, demonstrated mechanosensitive responses, and characterized their basic properties. Recordings were obtained using the mouse longitudinal muscle myenteric plexus preparation with patch-clamp and sharp intracellular electrodes. The neurons had an action potential hump and a slow afterhyperpolarization (AHP) current. The slow AHP was carried by intermediate conductance Ca 2ϩ-dependent K ϩ-channel currents sensitive to charybdotoxin and clotrimazole. All possessed a hyperpolarization-activated current that was blocked by extracellular cesium. They also expressed a TTX-resistant Na ϩ current with an onset near the resting potential. Pressing on the ganglion containing the patched neuron evoked depolarizing potentials in 17/18 cells. The potentials persisted after synaptic transmission was blocked. Volleys of presynaptic electrical stimuli evoked slow excitatory postsynaptic potentials (EPSPs) in 9/11 sensory neurons, but 0/29 cells received fast EPSP input. The slow EPSP was generated by removal of a voltageinsensitive K ϩ current. Patch-clamp recording with a KMeSO 4containing, but not a conventional KCl-rich, intracellular solution reproduced the single-spike slow AHPs and low input resistances seen with sharp intracellular recording. Cell-attached recording of intermediate conductance potassium channels supported the conclusion that the single-spike slow AHP is an intrinsic property of intestinal AH/sensory neurons. Unitary current recordings also suggested that the slow AHP current probably does not contribute significantly to the high resting background conductance seen in these cells. The characterization of mouse myenteric sensory neurons opens the way for the study of their roles in normal and pathological physiology.
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.
The Journal of physiology, 1988
1. The sources of inhibitory synaptic inputs to neurones in submucous ganglia of the guinea-pig small intestine were examined by making lesions to cause selective degeneration of nerve terminals of sympathetic or intrinsic origin. Intracellular recordings were used to evaluate the effects of lesions on the inhibitory inputs. Immunohistochemical techniques were used to identify the neurochemical classes of the impaled neurones and to confirm the efficacy of the lesions. 2. The neurones from which recordings were taken were filled with the fluorescent dye Lucifer Yellow. The preparations were then fixed and processed for immunohistochemistry. 3. Thirty-one neurones reactive for vasoactive intestinal polypeptide (VIP) were examined in control submucous ganglia and all exhibited inhibitory synaptic potentials. In preparations extrinsically denervated by severing the mesenteric nerves, twenty-seven of twenty-eight VIP-reactive neurones had inhibitory synaptic potentials. This indicates t...
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...
Characteristics of mucosally projecting myenteric neurones in the guinea-pig proximal colon
The Journal of Physiology, 1999
The NK_3 receptor antagonist SR 142801 (1 ìÒ) significantly decreased the amplitude and duration of the sEPSPs; the NK_1 receptor antagonist CP-99,994 (1 ìÒ) was ineffective. Atropine (0•5 ìÒ) increased the duration but not the amplitude of the sEPSPs. 5. Microejection of 100 mÒ sodium butyrate onto the neurones induced in 90% of the DiIlabelled neurones a transient depolarization associated with an increased excitability. In neurones with SHPs sodium butyrate evoked, additionally, a late onset hyperpolarization. Perfusion of 0•1-10 mÒ sodium butyrate induced a dose-dependent increase in neuronal excitability. Sodium butyrate was ineffective when applied directly onto the mucosa. 6. Mucosally projecting myenteric neurones of the colon are multipolar AH neurones with NK_3-mediated slow EPSPs and somal butyrate sensitivity.