Evidence that inhibitory motor neurons of the guinea-pig small intestine exhibit fast excitatory synaptic potentials mediated via P2X receptors

Johnson, Peter J.; Shum, Omar R.; Thornton, Peter D. J.; Bornstein, Joel C.

doi:10.1016/s0304-3940(99)00275-x

Cited by 47 publications

(65 citation statements)

References 15 publications

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“…The rat colon also shows purely nicotinic transmission between descending interneurons (5). In guinea pig ileum, transmission between the ascending interneurons is purely nicotinic (24), but there is a large nonnicotinic component between descending interneurons (22)(23)(24) that may be purinergic (46). In the present study, we also found a small purinergic component to transmission between descending interneurons, but this was not additive with the nicotinic component.…”

Section: Nicotinic Transmission Plays a Major Role In Distensionevokesupporting

confidence: 50%

Synaptic transmission in simple motility reflex pathways excited by distension in guinea pig distal colon

Bian

Heffer

Gwynne

et al. 2004

American Journal of Physiology-Gastrointestinal and Liver Physi

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We examined specific receptor/transmitter combinations used at functionally identified synapses in ascending and descending reflex pathways of guinea pig distal colon. Excitatory (EJPs) or inhibitory junction potentials (IJPs) were recorded intracellularly from nicardipine-paralyzed circular smooth muscle in either the oral or anal recording chamber of a three-chambered organ bath, respectively. Blockade of synaptic transmission in the central chamber with a 0.25 mM Ca 2ϩ /12 mM Mg 2ϩ solution abolished EJPs evoked by distension applied either in the central or the far (anal) chamber. IJPs evoked by distension in the central or the far (oral) chamber were depressed to ϳ50% of control. Hexamethonium (nicotinic receptor antagonist, 200 M) in the central chamber reduced IJPs evoked by far or central distension to 50%, whereas EJPs evoked by far distension were abolished and EJPs evoked by central distension were reduced to 70% of control. Hexamethonium in the recording chambers reduced both IJPs and EJPs evoked by central distension to ϳ50%. EJPs in the ascending pathway were unaffected by blockade of muscarinic receptors in the central chamber or blockade of neurokinin 3 tachykinin receptors in this or the recording chamber. In the descending pathway, blockade of P2 receptors in the same chambers had only a minor effect on distension-evoked IJPs. Thus some intrinsic sensory neurons of guinea pig colon have long descending projections (Ͼ30 mm), but ascending projections of Ͻ15 mm. In contrast to the ileum, transmission between ascending or descending interneurons and from sensory neurons to descending interneurons is predominantly via nicotinic receptors; but transmission to inhibitory or excitatory motoneurons and from sensory neurons to ascending interneurons involves nicotinic and other unidentified receptors. enteric nervous system; electrophysiology; smooth muscle; enteric reflex THE COLON IS SPECIALIZED FOR the absorption of water and electrolytes and the storage and transport of material. The digestion and absorption of nutrients (such as those produced from bacterial fermentation) is of lesser overall importance. The intrinsic circuitry underlying colonic behavior may thus be quite different from that of the small intestine in which mixing and primary nutrient absorption are crucial functions. These differences are currently not well defined but are critical for interpretation of a vast range of currently available data.The guinea pig small intestine has been an excellent model for studying the circuitry of the enteric nervous system. It is in this system that the best data on projection patterns, chemical code, and electrophysiology have been gathered and correlated to characterize specific functional classes of neuron (8) and to reveal the nature of synaptic transmission at specific classes of synapses (7). The circuitry of the ileum, in particular, provides a template on which to design studies investigating the circuitry in the colon.Neuroanatomical studies (31, 33, 34) have revealed substantial similar...

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Section: Nicotinic Transmission Plays a Major Role In Distensionevokesupporting

confidence: 50%

Synaptic transmission in simple motility reflex pathways excited by distension in guinea pig distal colon

Bian

Heffer

Gwynne

et al. 2004

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…10) [16,17], while there is only one class of ascending interneurons [16,17]. Second, while electrical stimulation evokes fast EPSPs mediated by nAChR in all S/uniaxonal neurons of the descending inhibitory pathway, many of these neurons also exhibit fast EPSPs mediated by either P2X or 5-HT 3 receptors [56,67,142]. Third, some sensory neurons have long anally projecting axons as well as circumferentially projecting axons [18], which complicates interpretation of data arising from pharmacological studies designed to isolate specific classes of synapses.…”

Section: Circuits Regulating Motility Reflexesmentioning

confidence: 99%

“…10) [5,56]. Although a component of transmission from the intrinsic sensory neurons responding to mucosal deformation involves NK 3 tachykinin receptors, a significant component of this transmission is unaffected by NK 3 receptor blockade [55].…”

Section: Circuits Regulating Motility Reflexesmentioning

confidence: 99%

Synaptic Transmission at Functionally Identified Synapses in the Enteric Nervous System: Roles for Both Ionotropic and Metabotropic Receptors

Gwynne

Bornstein²

2007

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Digestion and absorption of nutrients and the secretion and reabsorption of fluid in the gastrointestinal tract are regulated by neurons of the enteric nervous system (ENS), the extensive peripheral nerve network contained within the intestinal wall. The ENS is an important physiological model for the study of neural networks since it is both complex and accessible. At least 20 different neurochemically and functionally distinct classes of enteric neurons have been identified in the guinea pig ileum. These neurons express a wide range of ionotropic and metabotropic receptors. Synaptic potentials mediated by ionotropic receptors such as the nicotinic acetylcholine receptor, P2X purinoceptors and 5-HT 3 receptors are seen in many enteric neurons. However, prominent synaptic potentials mediated by metabotropic receptors, like the P2Y 1 receptor and the NK 1 receptor, are also seen in these neurons. Studies of synaptic transmission between the different neuron classes within the enteric neural pathways have shown that both ionotropic and metabotropic synaptic potentials play major roles at distinct synapses within simple reflex pathways. However, there are still functional synapses at which no known transmitter or receptor has been identified. This review describes the identified roles for both ionotropic and metabotropic neurotransmission at functionally defined synapses within the guinea pig ileum ENS. It is concluded that metabotropic synaptic potentials act as primary transmitters at some synapses. It is suggested identification of the interactions between different synaptic potentials in the production of complex behaviours will require the use of well validated computer models of the enteric neural circuitry.

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“…This is supported by a divided organ bath study, which found that PPADS depressed descending excitatory reflexes when in a chamber where it would act on synapses between interneurons but not on the muscle [125]. A surprising conclusion from these studies is that P2X receptors have no major role in ascending reflex pathways [159,161] or in transmission to longitudinal muscle motor neurons [35]. This is despite the fact that P2X 3 receptors are found in calretinin-immunoreactive neurons of guineapig ileum [147,148], which are either ascending interneurons or longitudinal muscle motor neurons [99].…”

Section: A 2bmentioning

confidence: 88%

“…This may be because PPADS is relatively ineffective in blocking P2Y 1 receptors negatively coupled to adenylyl cyclase [1]. Second, these studies have used divided organ baths that allow separate superfusion of different parts of reflex pathways running along the intestine [113,159]. The results show that in guinea-pig ileum, P2X receptors mediate transmission from descending interneurons to inhibitory motor neurons (Fig.…”

Section: P2 Receptors Within Enteric Neural Circuitsmentioning

confidence: 99%

Purinergic mechanisms in the control of gastrointestinal motility

Bornstein

2007

Purinergic Signalling

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For many years, ATP and adenosine have been implicated in movement regulation of the gastrointestinal tract. They act through three major receptor subtypes: adenosine or P1 receptors, P2X receptors and P2Y receptors. Each of these major receptor types can be subdivided into several different classes and is widely distributed amongst various neurons, muscle types, glia and interstitial cells that regulate intestinal functions. Several key roles for the different receptors and their endogenous ligands have been identified in physiological and pharmacological studies. For example, adenosine acting at A 1 receptors appears to inhibit intestinal motility in various pathological conditions. Similarly, ATP acting at P2Y receptors is an important component of inhibitory neuromuscular transmission, acting as a cotransmitter with nitric oxide. ATP acting at P2X and P2Y 1 receptors is important for synaptic transmission in simple descending excitatory and inhibitory reflex pathways. Some P2Y receptor subtypes prefer uridine nucleotides over purine nucleotides. Thus, roles for UTP and UDP as enteric transmitters in place of ATP cannot be excluded. ATP also appears to be important for sensory transduction, especially in chemosensitive pathways that initiate local inhibitory reflexes. Despite this evidence, data are lacking about the roles of either adenosine or ATP in more complex motility patterns such as segmentation or the interdigestive migrating motor complex. Clarification of roles for purinergic transmission in these common, but understudied, motility patterns will depend on the use of subtype-specific antagonists that in some cases have not yet been developed.

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Evidence that inhibitory motor neurons of the guinea-pig small intestine exhibit fast excitatory synaptic potentials mediated via P2X receptors

Cited by 47 publications

References 15 publications

Synaptic transmission in simple motility reflex pathways excited by distension in guinea pig distal colon

Synaptic transmission in simple motility reflex pathways excited by distension in guinea pig distal colon

Synaptic Transmission at Functionally Identified Synapses in the Enteric Nervous System: Roles for Both Ionotropic and Metabotropic Receptors

Purinergic mechanisms in the control of gastrointestinal motility

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