Intracellular recordings from cells in the myenteric plexus of the rat duodenum

Brookes, Simon J.; Ewart, W. R.; Dl, Wingate

doi:10.1016/0306-4522(88)90332-6

Cited by 30 publications

(24 citation statements)

References 33 publications

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“…Amplitudes of the monosynaptic fast EPSPs declined during stimulation of presynaptic neurons at frequencies above 0.5 Hz. Similar frequency-dependent declines in the amplitudes of fast EPSPs also occur in the myenteric plexus of guinea pigs (Nishi and North, 1973;Hanani and Bumstock, 1985) and rats (Brookes et al, 1988). Nishi and North (1973) suggested that the decrease results from decreased release of ACh rather than from decreased postsynaptic sensitivity to ACh because responses of postsynaptic neurons to ionophoretic application of ACh did not decrease.…”

Section: Resultsmentioning

confidence: 74%

“…This explanation seems especially plausible for synapses in cell cultures, where there is likely to be rapid dilution of neurally released substances. In freshly dissected myenteric plexus, multiple stimuli are usually necessary to evoke slow EPSPs, but single stimuli to nerve bundles sometimes evoke noncholinergic slow EPSPs (Morita and North, 1985;Brookes et al, 1988). It is not known whether the slow EPSPs evoked by such stimuli result from activation of more than one presynaptic neuron, nor is it known whether any of the neurons activated by such stimuli are dual-function neurons.…”

Section: Discussionmentioning

confidence: 99%

“…It is not known if VIP enhances muscarinic transmission in myenteric ganglia. Muscarinic synaptic potentials occur in guinea pig myenteric neurons but were not observed in rat myenteric plexus by Brookes et al (1988). Unfortunately, the postsynaptic neurons studied did not have detectable muscarinic responses to ACh (see also Willard and Nishi, 1985a), thereby precluding a test of whether VIP enhanced muscarinic responses.…”

Section: Discussionmentioning

confidence: 99%

“…The most useful preparations have been invertebrate nervous systems that contain reliably identifiable individual neurons (e.g., Adams and O'Shea, 1983;Bishop et al, 1987;Li and Calabrese, 1987) and those portions of the vertebrate peripheral nervous system that contain nearly homogeneous populations of presynaptic axons, such as visceromotor or autonomic preganglionic nerves (Jan et al, 1979(Jan et al, , 1983Lundberg et al, 1980;Jan and Jan, 1982). However, although there are several neuronal systems in which individual presynaptic axons elicit both fast and slow EPSPs (e.g., Dreyer and Chiapinelli, 1985;Brookes et al, 1988;Nusbaum and Marder, 1989) to date there is only one system, the bullfrog lumbar sympathetic ganglion, in which it has been possible to identify rigorously both a fast classical and a slow peptidergic cotransmitter at synaptic connections between neurons (Jan et al, 1979(Jan et al, , 1983Jan and Jan, 1982).…”

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confidence: 99%

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A vasoactive intestinal peptide-like cotransmitter at cholinergic synapses between rat myenteric neurons in cell culture

Willard

1990

J. Neurosci.

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Intracellular recording and immunochemical techniques were used to study synaptic transmission between individual pairs of rat myenteric plexus neurons in cell culture. This report describes the synaptic connections made by “dual function” presynaptic neurons that evoked slow postsynaptic depolarizations (slow EPSPs) in the same neurons in which they also evoked fast nicotinic cholinergic EPSPs. The slow EPSPs occurred only when presynaptic neurons were stimulated at frequencies of 5 Hz or higher. During the slow EPSPs, slope input resistance increased. The slow EPSPs were not detectably voltage-dependent, and they reversed sign at the estimated K+ equilibrium potential, suggesting that they resulted from a synaptically mediated decrease in resting K+ conductance. Several lines of evidence suggested that dual- function neurons evoke slow EPSPs by releasing a vasoactive intestinal peptide (VIP)-like cotransmitter. (1) Immunocytochemical staining revealed VIP-like immunoreactivity in all physiologically identified dual-function neurons. (2) Responses to exogenously applied VIP mimicked the slow EPSPs. (3) Superfusion of cultures with anti-VIP antisera blocked the slow EPSPs reversibly, as did application of desensitizing doses of VIP. These findings suggest that during periods of increased activity, subsets of cholinergic myenteric neurons release a VIP-like cotransmitter that enhances postsynaptic excitability. The effects of the cotransmitter may help to compensate for decreases in nicotinic EPSPs that occur during increased presynaptic activity.

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Section: Resultsmentioning

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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A vasoactive intestinal peptide-like cotransmitter at cholinergic synapses between rat myenteric neurons in cell culture

Willard

1990

J. Neurosci.

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“…Substance P also evokes slow depolarizations accompanied by decreased conductance in neurones of the adult rat myenteric plexus (Brookes, Ewart & Wingate, 1988). In contrast, a much more complex set of changes in ionic conductances occurs during slow EPSPs and responses to tachykinins in neurones of the guinea-pig IMG (Dun & Minota, 1981;Griffith, Hills & Brown, 1988) and the rat dorsal horn (Murase, Ryu & Randic, 1989).…”

Section: Conductance Changesmentioning

confidence: 99%

Substance P mediates synaptic transmission between rat myenteric neurones in cell culture.

Willard

1990

The Journal of Physiology

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SUMMARY1. Whole-cell patch-clamp recordings were made from pairs of neurones in cell cultures of rat myenteric neurones. In some pairs, action potentials evoked in the first neurone evoked a slow excitatory postsynaptic potential (EPSP) in the second neurone.2. Action potentials at a frequency of at least 5 Hz were required to evoke slow EPSPs. In one group of cells, the slow EPSP followed a series of nicotinic fast EPSPs; in another group, fast EPSPs did not precede the slow EPSP.3. The slow EPSPs were 2-16 mV in amplitude and were accompanied by decreased resting potassium conductance.4. Most (17/28) neurones in which action potentials evoked only slow EPSPs in a follower cell contained substance P (SP)-like immunoreactivity; they were not immunoreactive for 5-hydroxytryptamine (0/15) or vasoactive intestinal peptide (0/22

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Excitatory synaptic inputs on myenteric Dogiel type II neurones of the pig ileum

Cornelissen

Laet

Kroese

et al. 2001

J of Comparative Neurology

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The synaptic input on myenteric Dogiel type II neurones (n = 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 +/- 5 mV (mean +/- S.D.) and lasting 49 +/- 29 ms. The nicotinic nature of the fEPSPs was demonstrated by superfusing hexamethonium (20 microM). 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 +/- 9 mV, duration 7.0 +/- 7.2 seconds) as did 1,1-dimethyl-4-phenylpiperazinium iodide (DMPP) application (10 mM; 14 +/- 10 mV, duration 4.1 +/- 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 +/- 4 mV; duration 38.7 +/- 10.8 seconds). Immunostaining revealed 5-hydroxytryptamine hydrochloride (5-HT)- and calcitonin gene-related 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 nicotinic-like depolarisation (12 +/- 6 mV, duration 3.0 +/- 1.3 seconds) in 4 of 8 neurones tested, whereas microejection of CGRP (20 mM) gave rise to a slow muscarinic-like depolarisation (6 +/- 2 mV, duration 56.0 +/- 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.

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Intracellular recordings from cells in the myenteric plexus of the rat duodenum

Cited by 30 publications

References 33 publications

A vasoactive intestinal peptide-like cotransmitter at cholinergic synapses between rat myenteric neurons in cell culture

A vasoactive intestinal peptide-like cotransmitter at cholinergic synapses between rat myenteric neurons in cell culture

Substance P mediates synaptic transmission between rat myenteric neurones in cell culture.

Excitatory synaptic inputs on myenteric Dogiel type II neurones of the pig ileum

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