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Anatomy and Physiology of the Enteric Nervous System Gut: First Published As 10.1136/Gut.47.Suppl 4.Iv15 on 1 December 2000

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Anatomy and Physiology of the Enteric Nervous System Gut: First Published As 10.1136/Gut.47.Suppl 4.Iv15 on 1 December 2000 Gut 2000;(Suppl IV)47:iv15–iv19 iv15 Anatomy and physiology of the enteric nervous system Gut: first published as 10.1136/gut.47.suppl_4.iv15 on 1 December 2000. Downloaded from M Costa, S J H Brookes, G W Hennig The enteric nervous system (ENS) is a quasi and in the duodenum. It is on this spontane- autonomous part of the nervous system and ously active muscular apparatus that the includes a number of neural circuits that enteric motor circuits play their roles in control motor functions, local blood flow, shaping diVerent motor patterns. mucosal transport and secretions, and modu- The neural apparatus is composed of a large lates immune and endocrine functions. Al- number of enteric neurones that can be though these functions operate in concert and identified according to their location, neuro- are functionally interlinked, it is useful to con- chemistry, shape, projections, proportions, con- sider the neural circuits involved in each sepa- nections, and function. After intensive research rately.1 This short summary will concentrate from several laboratories over the past two dec- mainly on the neural circuits involved in motor ades, a full description of all functional classes of control.2 The enteric neural circuits are com- enteric neurones has been recently achieved in posed of enteric neurones arranged in networks the guinea pig small intestine (fig 1).6 The strat- of enteric ganglia connected by interganglionic egy included the development of methods com- strands. Most enteric neurones involved in bining immunohistochemistry, electrophysiol- motor functions are located in the myenteric ogy, retrograde tracing, neuronal filling, lesion plexus with some primary aVerent neurones techniques, and pharmacological analysis. located in the submucous plexus. As in all nervous systems involved in sensory-motor control, the ENS comprises primary aVerent The enteric neurones neurones, sensitive to chemical and mechanical PRIMARY AFFERENT NEURONES stimuli, interneurones and motorneurones that Primary aVerent neurones (also termed enteric act on the diVerent eVector cells including primary aVerent neurones (EPANs) or intrin- smooth muscle, pacemaker cells, blood vessels, sic primary aVerent neurones (IPANs)) are mucosal glands, and epithelia, and the distrib- present in both myenteric and submucous gan- uted system of intestinal cells involved in glia. They respond to luminal chemical stimuli, immune responses and endocrine and para- to mechanical deformation of the mucosa, and crine functions. to radial stretch and muscle tension. It is not The digestive tract is unique among internal yet clear whether epithelial cells such as organs because it is exposed to a large variety of enterochromaYn cells release substances, for http://gut.bmj.com/ physicochemical stimuli from the external instance serotonin, in response to chemical or world in the form of ingested food. As a conse- mechanical stimuli, to activate the endings of quence, the intestine has developed a rich rep- the primary aVerent neurones.7 They represent ertoire of coordinated movements of its about 30% of myenteric neurones and 14% of muscular apparatus to ensure the appropriate submucosal neurones, have a distinct Dogiel mixing and propulsion of contents during type II shape and have a long after hyperpolari- digestion, absorption, and excretion. The sation following action potentials. All of these on October 2, 2021 by guest. Protected copyright. oro-aboral transit of the intestinal contents can neurones project to the villi and branch within be regarded as a form of adaptive locomotion the submucous and myenteric ganglia locally. that occurs over a wide range of spatial and A proportion of these neurones (10% of temporal domains.3 The movements of the primary aVerent neurones) also have long intestine are the result of interaction of the descending projections to aboral myenteric neural apparatus and the muscular apparatus.4 ganglia.8 They receive slow synaptic input The muscular apparatus is organised in (probably mediated by tachykinins) from other muscle layers made up of large collections of primary aVerent neurones to form reciprocally smooth muscle cells interconnected electrically innervated networks. They project circumfer- via gap junctions to operate as larger functional entially to synapse with myenteric ascending mechanical units. The membrane potential of interneurones, descending interneurones, long- smooth muscle is driven to oscillate (slow itudinal muscle motorneurones, excitatory waves) by a syncytial network of pacemaker circular muscle motorneurones, and inhibitory Department of cells (interstitial cells of Cajal) probably also circular muscle motorneurones. It is likely that Physiology and Centre via gap junctions.5 As the action potentials of diVerent subpopulations are connected sepa- of Neuroscience, the smooth muscles, and thus their associated rately, with ascending and descending path- Flinders University, ways. SA Australia muscle contraction, do not appear to propagate M Costa over long distances, the coordination of muscle S J H Brookes activity over long distances is highly dependent G W Hennig on the spatiotemporal patterns of the slow wave Abbreviations used in this paper: ENS, enteric nervous system; EPANs, enteric primary aVerent generated by the pacemaker networks. The Correspondence to: neurones; IPANs, intrinsic primary aVerent neurones; Professor M Costa. myogenic patterns of activity can support pro- ChAT, choline acetyltransferase; VIP, vasoactive marcello.costa@flinders.edu.au pulsive behaviour, for example in the antrum intestinal peptide; NOS, nitric oxide synthase. www.gutjnl.com iv16 Costa, Brookes, Hennig EXCITATORY CIRCULAR MUSCLE ASCENDING INTERNEURONES MOTORNEURONES This small (5%) but most important class of Gut: first published as 10.1136/gut.47.suppl_4.iv15 on 1 December 2000. Downloaded from These represent the final motor output to the enteric neurones belongs to the Dogiel type I circular muscle (14%), have a Dogiel type I morphology, and receives fast synaptic inputs shape, receive fast nicotinic and probably slow from other ascending interneurones which synaptic input from local primary aVerent neu- form a chain of ascending excitation. They also rones, and from the only class of cholinergic receive fast nicotinic and slow synaptic inputs ascending interneurones. They also appear to from enteric primary aVerent neurones. They receive excitatory inputs from descending project orally within the myenteric plexus to interneurones. They project to the circular synapse with the final excitatory circular mus- muscle where they form a denser arrangement cle motor neurones via fast nicotinic and non- of nerve endings in the deep muscular plexus. cholinergic slow synaptic inputs. They contain They use acetylcholine and tachykinins as not only the enzyme for the synthesis of acetyl- transmitters acting directly on smooth muscle choline but also tachykinins and opioid pep- and possibly indirectly via the network of inter- tides.13 stitial cells in the deep muscular plexus.9–11 DESCENDING INTERNEURONES INHIBITORY CIRCULAR MUSCLE MOTORNEURONES There are several classes of descending in- These Dogiel type I neurones (17%) receive terneurones that comprise about 7% of the fast nicotinic inputs from primary aVerent total.614 Three of these are probably choliner- neurones and non-cholinergic inputs from the gic as they contain the enzyme for the synthe- long descending primary aVerent neurones. sis of acetylcholine, choline acetyltransferase They project to the circular muscle where their (ChAT). Each diVers in their neurochemistry. axons are intimately associated with those of Somatostatin and ChAT containing descend- the excitatory motorneurones in the deep mus- ing interneurones (4%) have a filamentous cular plexus. They use multiple mechanisms of shape, receive fast and slow synaptic inputs inhibitory transmission including nitric oxide, mainly from non-primary aVerent neurones, adenosine triphosphate, and the peptides and form a chain of interconnected interneu- vasoactive intestinal peptide (VIP) and pitui- rones synapsing with other somatostatin neu- tary activating cyclic AMP peptide acting rones and with other myenteric and submu- directly on smooth muscle or indirectly via cous neurones. Serotonin and ChAT interstitial cells.911 containing neurones (2%) project aborally to other myenteric and submucosal neurones but LONGITUDINAL MUSCLE MOTORNEURONES not to inhibitory motorneurones. Whether This relatively large class (25%) of small these neurones use serotonin in addition to neurones with short projections to the longitu- acetylcholine remains to be confirmed. Serot- dinal muscle receive synaptic inputs from the onin may act via fast ion channel gated recep- enteric primary aVerent neurones and from tors or via slow G protein linked receptors. 12 ascending and descending pathways. Nitric oxide synthase (NOS), VIP, and ChAT http://gut.bmj.com/ LM IN LMMN AN DIN on October 2, 2021 by guest. Protected copyright. MP EPAN CM EMN IMN F′ SMP Mucosa Oral Anal Figure 1 Classes of myenteric neurones. LM, longitudinal muscle; CM, circular muscle; MP,myenteric plexus; SMP, submucous plexus; AN, ascending neurones; IN, intestinofugal neurones; DIN, descending interneurones; EPAN, enteric primary aVerent neurones; EMN, excitatory motorneurones; IMN, inhibitory motorneurones; LMMN, longitudinal motorneurones. The secretomotor and vasomotor neurones in the myenteric and submucous plexuses are not labelled (modified from Costa and colleagues6).
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