Development of extrinsic innervation in the abdominal intestines of human embryos. 2020

Nutmethee Kruepunga, and Jill P J M Hikspoors, and Cindy J M Hülsman, and Greet M C Mommen, and S Eleonore Köhler, and Wouter H Lamers
Department of Anatomy & Embryology, Maastricht University, Maastricht, The Netherlands.

Compared to the intrinsic enteric nervous system (ENS), development of the extrinsic ENS is poorly documented, even though its presence is easily detectable with histological techniques. We visualised its development in human embryos and foetuses of 4-9.5 weeks post-fertilisation using Amira 3D-reconstruction and Cinema 4D-remodelling software. The extrinsic ENS originated from small, basophilic neural crest cells (NCCs) that migrated to the para-aortic region and then continued ventrally to the pre-aortic region, where they formed autonomic pre-aortic plexuses. From here, nerve fibres extended along the ventral abdominal arteries and finally connected to the intrinsic system. Schwann cell precursors (SCPs), a subgroup of NCCs that migrate on nerve fibres, showed region-specific differences in differentiation. SCPs developed into scattered chromaffin cells of the adrenal medulla dorsolateral to the coeliac artery (CA) and into more tightly packed chromaffin cells of the para-aortic bodies ventrolateral to the inferior mesenteric artery (IMA), with reciprocal topographic gradients between both fates. The extrinsic ENS first extended along the CA and then along the superior mesenteric artery (SMA) and IMA 5 days later. Apart from the branch to the caecum, extrinsic nerves did not extend along SMA branches in the herniated parts of the midgut until the gut loops had returned in the abdominal cavity, suggesting a permissive role of the intraperitoneal environment. Accordingly, extrinsic innervation had not yet reached the distal (colonic) loop of the midgut at 9.5 weeks development. Based on intrinsic ENS-dependent architectural remodelling of the gut layers, extrinsic innervation followed intrinsic innervation 3-4 Carnegie stages later.

UI MeSH Term Description Entries
D007422 Intestines The section of the alimentary canal from the STOMACH to the ANAL CANAL. It includes the LARGE INTESTINE and SMALL INTESTINE. Intestine
D009432 Neural Crest The two longitudinal ridges along the PRIMITIVE STREAK appearing near the end of GASTRULATION during development of nervous system (NEURULATION). The ridges are formed by folding of NEURAL PLATE. Between the ridges is a neural groove which deepens as the fold become elevated. When the folds meet at midline, the groove becomes a closed tube, the NEURAL TUBE. Neural Crest Cells,Neural Fold,Neural Groove,Cell, Neural Crest,Cells, Neural Crest,Crest, Neural,Crests, Neural,Fold, Neural,Folds, Neural,Groove, Neural,Grooves, Neural,Neural Crest Cell,Neural Crests,Neural Folds,Neural Grooves
D002454 Cell Differentiation Progressive restriction of the developmental potential and increasing specialization of function that leads to the formation of specialized cells, tissues, and organs. Differentiation, Cell,Cell Differentiations,Differentiations, Cell
D002465 Cell Movement The movement of cells from one location to another. Distinguish from CYTOKINESIS which is the process of dividing the CYTOPLASM of a cell. Cell Migration,Locomotion, Cell,Migration, Cell,Motility, Cell,Movement, Cell,Cell Locomotion,Cell Motility,Cell Movements,Movements, Cell
D006801 Humans Members of the species Homo sapiens. Homo sapiens,Man (Taxonomy),Human,Man, Modern,Modern Man
D017615 Enteric Nervous System Two ganglionated neural plexuses in the gut wall which form one of the three major divisions of the autonomic nervous system. The enteric nervous system innervates the gastrointestinal tract, the pancreas, and the gallbladder. It contains sensory neurons, interneurons, and motor neurons. Thus the circuitry can autonomously sense the tension and the chemical environment in the gut and regulate blood vessel tone, motility, secretions, and fluid transport. The system is itself governed by the central nervous system and receives both parasympathetic and sympathetic innervation. (From Kandel, Schwartz, and Jessel, Principles of Neural Science, 3d ed, p766) Enteric Nervous Systems,Nervous System, Enteric,Nervous Systems, Enteric,System, Enteric Nervous,Systems, Enteric Nervous
D047108 Embryonic Development Morphological and physiological development of EMBRYOS. Embryo Development,Embryogenesis,Postimplantation Embryo Development,Preimplantation Embryo Development,Embryonic Programming,Post-implantation Embryo Development,Postnidation Embryo Development,Postnidation Embryo Development, Animal,Pre-implantation Embryo Development,Prenidation Embryo Development, Animal,Development, Embryo,Development, Embryonic,Development, Postnidation Embryo,Embryo Development, Post-implantation,Embryo Development, Postimplantation,Embryo Development, Postnidation,Embryo Development, Pre-implantation,Embryo Development, Preimplantation,Embryonic Developments,Embryonic Programmings,Post implantation Embryo Development,Pre implantation Embryo Development
D038081 Organogenesis Formation of differentiated cells and complicated tissue organization to provide specialized functions.

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