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Development of extrinsic innervation in the abdominal intestines of human embryos
Author(s) -
Kruepunga Nutmethee,
Hikspoors Jill P. J. M.,
Hülsman Cindy J. M.,
Mommen Greet M. C.,
Köhler S. Eleonore,
Lamers Wouter H.
Publication year - 2020
Publication title -
journal of anatomy
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 0.932
H-Index - 118
eISSN - 1469-7580
pISSN - 0021-8782
DOI - 10.1111/joa.13230
Subject(s) - anatomy , biology , neural crest , inferior mesenteric artery , superior mesenteric artery , pathology , medicine , embryo , microbiology and biotechnology
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.