Local Neural Control of Intestinal Motility: Nerve Circuits Deduced for the Guinea‐pig Small Intestine

Abstract

1. Propulsion of digesta along the intestine appears to occur by the action of a series of local reflexes which cause contraction oral to the digesta and relaxation of circular muscle on the anal side. 2. There is now substantial evidence available about the identities of the enteric neurons that mediate these reflexes. 3. The motor neurons and interneurons of the reflex pathways lie within the myenteric plexus. These neurons can be classified electrophysiologically as S-neurons and have distinctive projections and neurochemistries. 4. The sensory neurons may lie in the myenteric plexus, but there is some evidence for sensory neurons in the submucous plexus. A contribution from extrinsic sensory neurons to local motility reflexes cannot be ruled out. Intrinsic sensory neurons are probably AH-neurons and are large multi-axonal cells.

Glutamatergic Enteric Neurons

“…"Shellfish poisoning," which is caused by the ingestion of mussels contaminated by domoic acid, a potent ionotropic non-NMDA receptor agonist, is characterized by severe gastrointestinal distress (nausea, vomiting, and diarrhea) (Perl et al, 1990). We now report, for the first time, that glutamate mediates excitatory synaptic transmission in enteric neurons, that enteric neurons express the neuronal glutamate transporter, EAAC1, NMDA, and non-NMDA (AMPA) receptors, and that a subset of enteric neurons that previously have been demonstrated to be sensory (Kirchgessner et al, 1992;Bornstein, 1994) are glutamatergic. These findings are consistent with the idea that glutamate is an excitatory enteric neurotransmitter and support the possibility that intrinsic sensory neurons use glutamate as a transmitter.…”

Analysis of contributions of acetylcholine and tachykinins to neuro‐neuronal transmission in motility reflexes in the guinea‐pig ileum

“…These polarized reflexes sensory neurones, interneurones and motor neurones recan be activated by distension of the gut wall or by mechanical sponsible for these reflexes are intrinsic to the enteric nervous or chemical stimulation of the mucosa (Bayliss & Starling, system. Indeed, most of the neuro-neuronal connections are 1899; Hukuhara et al, 1958; probably contained within the myenteric plexus (Bornstein, 1994). While the basic elements of motility reflex circuits have been characterized electrophysiologically and anatomically (Costa 1Author for correspondence.…”

“…While the basic elements of motility reflex circuits have been characterized electrophysiologically and anatomically (Costa 1Author for correspondence. et al, 1992;Bornstein, 1994;Furness et al, 1994), the phar2Present address: Department of Human Physiology, Flinders macology of transmission within these pathways remains unMedical Centre, Bedford Park, SA 5042, Australia certain. Nicotinic receptor antagonists abolish propulsion of British Journal of Pharmacology (1996) 118, [973][974][975][976][977][978][979][980][981][982][983] intestinal content in intact preparations, indicating that acetylcholine (ACh) acting at nicotinic synapses is essential for peristalsis (Crema et al, 1970;Costa & Furness, 1976;Yagasaki et al, 1979;Tonini et al, 1981).…”

Nicotinic mechanisms in the autonomic control of organ systems

“…In one subset of S neurons, fast synaptic transmission is exclusively mediated by nAChRs; whereas in the other two subsets fast excitatory post synaptic potentials (fEPSP) can be mediated by ATP or 5-hydroxytriptamine (5-HT) in addition to ACh. AH cells are sensory neurons (Bornstein, 1994;Costa et al, 1996). In these neurons AMPA receptor-mediated glutamatergic fEPSPs have been recorded in addition to those mediated by ACh at nAChRs .…”

“…S neurons display multiple fast excitatory postsynaptic potentials, whereas AH neurons are characterized by long-lasting afterhyperpolarization following an action potential. The S category comprises interneurons and motorneurons grouped in three subsets (Bornstein, 1994;Costa et al, 1996). In one subset of S neurons, fast synaptic transmission is exclusively mediated by nAChRs; whereas in the other two subsets fast excitatory post synaptic potentials (fEPSP) can be mediated by ATP or 5-hydroxytriptamine (5-HT) in addition to ACh.…”