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[Background and evoked neuronal activity of ganglia in the submucous plexus of the small intestine].

In preparations of the cat small intestine, presence of three types of cells was revealed: 1st--with single spikes, 2nd--with slow, and 3rd--with fast bursts of spontaneous activity as well as groups of silent neurons. The 1st and the 2nd type cells and some silent cells receive activating influence from adjacent ganglia. Silent neurons included mechanosensitive cells responding with specific series of discharges to mechanical deformation of the ganglion and to electric stimulation of adjacent ganglia. The interneuronal relationships within the ganglion and connections between cells of adjacent ganglia were revealed which suggests that all neurons of the plexus are involved in a functional network.

Acetylcholine↗

Observations on the actions of substance P and [D-Arg1,D-Pro2,D-Trp7,9,Leu11)substance P on single neurons of the guinea pig submucous plexus.

Intracellular recordings were made from neurons of the guinea pig submucosal plexus and the effects of substance P and the substance P analogue [D-Arg1,D-Pro2,D-Trp7,9,Leu11]substance P were examined. Substance P (20-200 nM) depolarized all submucosal neurons; these depolarizations were shown to be due to a decrease in the resting (or "leak") potassium conductance of the membrane. In approximately 50% of the 46 neurons tested, superfusion with [D-Arg1,D-Pro2,D-Trp7,9,Leu11]substance P (0.2-20 microM) produced a dose-dependent membrane hyperpolarization. This hyperpolarization was prevented by the alpha 2-adrenoceptor antagonist idazoxan (300 nM) or by concentrations of cobalt which abolished all spontaneous and evoked synaptic potentials, indicating that it resulted from release of noradrenaline from sympathetic nerve terminals. [D-Arg1,D-Pro2,D-Trp7,9,Leu11]substance P depressed the amplitude of the three synaptic potentials recorded from submucosal neurons; the concentrations that caused 50% of the maximal inhibition of the fast excitatory postsynaptic potential, the inhibitory postsynaptic potential, and slow excitatory postsynaptic potential were 40 microM, 600 nM and 20 microM, respectively. When idazoxan was present, the substance P analogue was less effective in depressing the amplitudes of the fast and slow excitatory synaptic potentials suggesting that much of its presynaptic inhibition also resulted from release of noradrenaline. These results provide evidence that [D-Arg1,D-Pro2,D-Trp7,9,Leu11]substance P releases noradrenaline from sympathetic nerves in the submucosal plexus. One effect of this is a membrane hyperpolarization; another is a presynaptic inhibition of transmitter release. These actions much limit the usefulness of this "substance P antagonist" in efforts to show that synaptic potentials, such as the slow excitatory synaptic potential, are mediated by substance P.

Animals↗

An electrophysiological comparison of substance P-immunoreactive neurons with other neurons in the guinea-pig submucous plexus.

Intracellular microelectrodes containing the dye Lucifer yellow CH were used to record from nerve cells of ganglia in isolated preparations of submucosa from the guinea-pig small intestine. The electrophysiological properties of the neurons were investigated by passing intracellular current pulses and by stimulating nerve strands that connect with the ganglia. Following each electrophysiological investigation, the fluorescent dye was injected into the neuron by passing hyperpolarizing currents through the electrode. The preparations were fixed and processed for substance P (SP) immunohistochemistry. When impaled neurons were not immunoreactive for SP the preparations were processed first for vasoactive intestinal peptide immunoreactivity and then for neuropeptide Y immunoreactivity. Data from neurons reactive for either of these peptides were pooled for comparison with the data from SP-immunoreactive neurons. Nerve cells that were immunoreactive for SP were usually multipolar, had broad action potentials (half width 2.6 ms compared with 1.5 ms for other submucous neurons) and lower input resistances than other submucous neurons. Only a minority (6 of 18) had demonstrable fast excitatory synaptic inputs. When such excitatory synaptic inputs were observed, these did not initiate action potentials. Thus, the SP-immunoreactive neurons were readily distinguishable from other submucous neurons. It is concluded that these neurons are likely to be sensory.

Animals↗

A special type of ganglion cells in the submucous plexus of mouse small intestine.

The perikarya of sensory neurons have been reported frequently from electrophysiological studies of the plexus submucosus of many mammalian digestive tracts, but the fine structural characteristics of those cells or ganglia have rarely been demonstrated. Therefore, we conducted an electron microscopic study in search of possible sensory perikarya in the plexus of the mouse small intestine. Many ganglion cells scattered over the plexus submucosus possessed a few areas of fine granules frequently adjacent to dense bodies in their perikaryonal cytoplasm, as revealed first by Wilson et al. [23], who were unable to explain the significance, of this finding. On the other hand, one type of ganglion with a special three-dimensional structure was observed in the same plexus. This ganglion was composed of one central perikaryon, one innermost cellular semiperfect cover of the Schwann cell, a middle two-layered cellular coat, an outer neuropil and an outermost external lamina. The surface of the central perikaryon, which differed from those of the other ganglion cells, was almost entirely covered with one Schwann cell, most probably for isolation from various kinds of external electrical and/or chemical inputs. Dumbbell-shaped vesicles containing endings that were presumed to be sensory, were frequently localized in the outer neuropil of this ganglion. It is likely that this perikaryon belongs to the sensory ganglion cells and so acts as an important factor in the peristaltic reflex arc.

Animals↗

Melatonin modulates cholinergic transmission by blocking nicotinic channels in the guinea-pig submucous plexus.

Melatonin, a hormone produced and released by the pineal gland is also synthesized by cells of the gastrointestinal wall, where it might be a local regulator of gut functions. In this study, we investigated the possible role of melatonin as a modulator of the enteric nervous system. Intracellular recordings were made in neurons of the submucosal plexus from the guinea-pig ileum to measure the melatonin effects on their electrophysiological properties. Melatonin did not alter the membrane potential, the membrane resistance and the noradrenergic inhibitory postsynaptic potentials. However, melatonin (30-3000 microM) reversibly decreased the amplitude of nicotinic excitatory postynaptic potentials (EPSPs) in a concentration-dependent manner (IC50 = 247 microM). These actions of melatonin were not modified by the presence of idazoxan and atropine indicating that they are not mediated by endogenous release of acetylcholine, noradrenaline, or by direct activation of alpha 2-adrenoceptors or muscarinic receptors. The superfusion of melatonin also blocked the nicotinic depolarizations induced by locally applied acetylcholine, indicating that at least part of its effects are postsynaptic. In voltage-clamp experiments, using the whole-cell configuration, melatonin also inhibited the nicotinic inward currents induced by acetylcholine (IACh) in a concentration-dependent manner (IC50 = 257 microM). Melatonin decreased the maximal IACh but did not affect the potency of acetylcholine to induce this current, indicating a noncompetitive antagonism. This effect was voltage-dependent. Our observations indicate that melatonin inhibits the fast EPSPs by directly and specifically blocking the nicotinic channels. The relative high concentrations of melatonin required to produce such an effect rules this out as one of its humoral actions. Such an effect, however, might be of physiological significance close to the cells that release melatonin in the gastrointestinal wall or in other organs.

Acetylcholine↗

Post- and presynaptic effects of norepinephrine in guinea-pig colonic submucous plexus.

Intracellular recording techniques were used to investigate the effects of norepinephrine on submucous neurones in the guinea-pig distal colon. In 81% of the neurones, pressure microejection of norepinephrine produced a membrane hyperpolarization associated with a decrease in excitability and input resistance. Microejection of clonidine (1 microM) mimicked the norepinephrine-induced hyperpolarization, whereas both phentolamine (1 microM) and yohimbine (1 microM) reversibly suppressed it. Superfusion of norepinephrine (1 nM - 10 microM) hyperpolarized the cells in a concentration-dependent manner. Norepinephrine and clonidine (1 nM - 10 microM) caused a concentration-dependent presynaptic inhibition of stimulus-evoked cholinergic fast excitatory postsynaptic potential. Slow inhibitory post-synaptic potentials (sISPSs) were induced by focal electrical stimulation of the interganglionic fibre tracts in 43% of the neurones tested. Superfusion of both phentolamine (1 microM) and yohimbine (1 microM) reduced the sIPSPs while prazosin (1 microM) had no significant effect. We concluded that norepinephrine acted post- and presynaptically via alpha 2-adrenoreceptors to have an inhibitory effect on the guinea-pig colonic submucous. In addition, our study strongly supported the role of norepinephrine as a mediator of the sIPSPs. As a result, norepinephrine would primarily suppress information transfer within the neuronal circuits in guinea-pig colonic submucosal plexus.

Acetylcholine↗

[The vascularization of the submucous external plexus (Schabadasch) and the submucous internal plexus (Meissner) in the small intestine of swine and cat].

Each ganglion of the plexus Schabadasch is supplied by a specific periganglionic capillary network. Within the plexus Meissner, several ganglia are connected to circulation areas. The communicating branches of the plexus Schabadasch have their own capillary system; as to the plexus Meissner, this is valid for the cat only. The results allow to conclude that the centres of the intramural nervous system of the intestinal wall are equipped with a preferred and self-acting vascularization.

Anatomy, Comparative↗