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Structure and Neurochemical Organization of the Enteric Nervous System

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Abstract

The sections in this article are:

1 Histochemical Analysis of Circuitry of Enteric Nervous System
2 Nerve Cell Bodies in Enteric Ganglia
3 Distribution of Nerve Fibers
4 Direct Tracing of Enteric Neuron Projections
5 Effects of Lesions
6 Retrograde‐Transport Tracing of Enteric Nerve Pathways
7 Projections of Enteric Neurons to Specific Targets and Functional Correlations
7.1 Guinea Pig Small Intestine Circular Muscle
7.2 Longitudinal Muscle
7.3 Myenteric Ganglia of Guinea Pig Small Intestine
7.4 Submucous Ganglia in Guinea Pig Small Intestine
7.5 Mucosa
7.6 Blood Vessels
7.7 Prevertebral Ganglia
7.8 Projections of Enteric Neurons in Other Species
8 Conclusions
Figure 1. Figure 1.

Schematic of projections of enteric motoneurons that supply circular muscle in guinea pig small intestine. Excitatory motoneurons ( + ) project to circular muscle located more orally or underneath nerve cell bodies of origin. They all contain substance P (SP) and some of them also contain enkephalins (ENK). Some or all of these excitatory neurons are cholinergic. Two types of inhibitory motoneurons ( — ) supply circular muscle, one with a short and other with a long anal projection. Functional role of SP‐vasoactive intestinal peptide (VIP) neurons is not known. Ach, acetylcholine; CM, circular muscle; DYN, dynorphin; GRP, gastrin‐releasing peptide; MP, myenteric plexus; NPY, neuropeptide Y.

Figure 2. Figure 2.

Diagram of projections of histochemically identified myenteric neurons within myenteric plexus along longitudinal axis of guinea pig small intestine. Only relative lengths of projections are indicated, and these range from very short, i.e., within one row of myenteric ganglia (<1 mm) for SP, calcium‐binding proteins (CaBP), and short somatostatin (SOM) neurons, to 15 mm for serotonin (5‐HT) neurons. CCK, cholecystokinin; GAL, galanin. For other abbrevations, see Fig. 1.

Figure 3. Figure 3.

Schematic of functional input and output of guinea pig submucous ganglia and their probable neurochemical correlates. +, Excitatory input; ‐, inhibitory input. CGRP, calcitonin gene‐related peptide; M, mucosa; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.

Figure 4. Figure 4.

Schematic of projections of nerve fibers to submucous ganglia. A number of histochemical markers are found in neurons that project to submucous ganglia. Some of these myenteric neurons project directly to underlying submucous neurons, whereas others first run anally within myenteric plexus before diving to submucous ganglia. Because pattern of coexistance of histochemical markers in these projections has not been established, they are only listed above ganglia of origin. CGRP, calcitonin gene‐related peptide; ChAT, choline acetyltransferase; DRG, dorsal root ganglia; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.

Figure 5. Figure 5.

Diagram of different types of neurons projecting to mucosa of guinea pig small intestine. CGRP, calcitonin gene‐related peptide; ChAT, choline acetyltransferase; DRG, dorsal root ganglia; M, mucosa; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.

Figure 6. Figure 6.

Schematic of neurochemical types of nerve fibers supplying submucous blood vessels in guinea pig small intestine. Nerve fibers of extrinsic origin reach submucosa following mesenteric blood vessels as they cross external layers of intestine. CGRP, calcitonin gene‐related peptide; DRG, dorsal root ganglia; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.

Figure 7. Figure 7.

Schematic of projections of myenteric neurons within myenteric plexus in rat small intestine. CGRP, calcitonin gene‐related peptide. For other abbreviations, see Fig. 1 and 2.

Redrawn from Ekblad et al. 31


Figure 1.

Schematic of projections of enteric motoneurons that supply circular muscle in guinea pig small intestine. Excitatory motoneurons ( + ) project to circular muscle located more orally or underneath nerve cell bodies of origin. They all contain substance P (SP) and some of them also contain enkephalins (ENK). Some or all of these excitatory neurons are cholinergic. Two types of inhibitory motoneurons ( — ) supply circular muscle, one with a short and other with a long anal projection. Functional role of SP‐vasoactive intestinal peptide (VIP) neurons is not known. Ach, acetylcholine; CM, circular muscle; DYN, dynorphin; GRP, gastrin‐releasing peptide; MP, myenteric plexus; NPY, neuropeptide Y.



Figure 2.

Diagram of projections of histochemically identified myenteric neurons within myenteric plexus along longitudinal axis of guinea pig small intestine. Only relative lengths of projections are indicated, and these range from very short, i.e., within one row of myenteric ganglia (<1 mm) for SP, calcium‐binding proteins (CaBP), and short somatostatin (SOM) neurons, to 15 mm for serotonin (5‐HT) neurons. CCK, cholecystokinin; GAL, galanin. For other abbrevations, see Fig. 1.



Figure 3.

Schematic of functional input and output of guinea pig submucous ganglia and their probable neurochemical correlates. +, Excitatory input; ‐, inhibitory input. CGRP, calcitonin gene‐related peptide; M, mucosa; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.



Figure 4.

Schematic of projections of nerve fibers to submucous ganglia. A number of histochemical markers are found in neurons that project to submucous ganglia. Some of these myenteric neurons project directly to underlying submucous neurons, whereas others first run anally within myenteric plexus before diving to submucous ganglia. Because pattern of coexistance of histochemical markers in these projections has not been established, they are only listed above ganglia of origin. CGRP, calcitonin gene‐related peptide; ChAT, choline acetyltransferase; DRG, dorsal root ganglia; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.



Figure 5.

Diagram of different types of neurons projecting to mucosa of guinea pig small intestine. CGRP, calcitonin gene‐related peptide; ChAT, choline acetyltransferase; DRG, dorsal root ganglia; M, mucosa; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.



Figure 6.

Schematic of neurochemical types of nerve fibers supplying submucous blood vessels in guinea pig small intestine. Nerve fibers of extrinsic origin reach submucosa following mesenteric blood vessels as they cross external layers of intestine. CGRP, calcitonin gene‐related peptide; DRG, dorsal root ganglia; NA, norepinephrine; PG, prevertebral ganglia; SM, submucosa. For other abbreviations, see Fig. 1 and 2.



Figure 7.

Schematic of projections of myenteric neurons within myenteric plexus in rat small intestine. CGRP, calcitonin gene‐related peptide. For other abbreviations, see Fig. 1 and 2.

Redrawn from Ekblad et al. 31
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Marcello Costa, John B Furness. Structure and Neurochemical Organization of the Enteric Nervous System. Compr Physiol 2011, Supplement 17: Handbook of Physiology, The Gastrointestinal System, Neural and Endocrine Biology: 97-109. First published in print 1989. doi: 10.1002/cphy.cp060205