Sympathetic Pathways Target Cholinergic Neurons in the Human Colonic Myenteric Plexus.
colon
enteric nervous system
gastrointestinal motility
human
myenteric plexus
sympathetic nervous system
Journal
Frontiers in neuroscience
ISSN: 1662-4548
Titre abrégé: Front Neurosci
Pays: Switzerland
ID NLM: 101478481
Informations de publication
Date de publication:
2022
2022
Historique:
received:
27
01
2022
accepted:
21
02
2022
entrez:
4
4
2022
pubmed:
5
4
2022
medline:
5
4
2022
Statut:
epublish
Résumé
The sympathetic nervous system inhibits human colonic motility largely by effects on enteric neurons. Noradrenergic axons, which branch extensively in the myenteric plexus, are integral to this modulatory role, but whether they contact specific types of enteric neurons is unknown. The purpose of this study was to determine the association of noradrenergic varicosities with types of enteric neurons. Human colonic tissue from seven patients was fixed and dissected prior to multi-layer immunohistochemistry for human RNA binding proteins C and D (HuC/D) (pan-neuronal cell body labelling), tyrosine hydroxylase (TH, catecholaminergic labelling), Enkephalin (ENK), choline acetyltransferase (ChAT, cholinergic labelling) and/or nitric oxide synthase (NOS, nitrergic labelling) and imaged using confocal microscopy. TH-immunoreactive varicose nerve endings and myenteric cell bodies were reconstructed as three dimensional digital images. Data was exported to a purpose-built software package which quantified the density of varicosities close to the surface of each myenteric cell body. TH-immunoreactive varicosities had a greater mean density within 1 μm of the surface of ChAT +/NOS- nerve cell bodies compared with ChAT-/NOS + cell bodies. Similarly, ENK-immunoreactive varicosities also had a greater mean density close to ChAT +/NOS- cell bodies compared with ChAT-/NOS + cells. A method for quantifying close associations between varicosities and nerve cell bodies was developed. Sympathetic axons in the myenteric plexus preferentially target cholinergic excitatory cells compared to nitrergic neurons (which are largely inhibitory). This connectivity is likely to be involved in inhibitory modulation of human colonic motility by the sympathetic nervous system.
Sections du résumé
Background
UNASSIGNED
The sympathetic nervous system inhibits human colonic motility largely by effects on enteric neurons. Noradrenergic axons, which branch extensively in the myenteric plexus, are integral to this modulatory role, but whether they contact specific types of enteric neurons is unknown. The purpose of this study was to determine the association of noradrenergic varicosities with types of enteric neurons.
Methods
UNASSIGNED
Human colonic tissue from seven patients was fixed and dissected prior to multi-layer immunohistochemistry for human RNA binding proteins C and D (HuC/D) (pan-neuronal cell body labelling), tyrosine hydroxylase (TH, catecholaminergic labelling), Enkephalin (ENK), choline acetyltransferase (ChAT, cholinergic labelling) and/or nitric oxide synthase (NOS, nitrergic labelling) and imaged using confocal microscopy. TH-immunoreactive varicose nerve endings and myenteric cell bodies were reconstructed as three dimensional digital images. Data was exported to a purpose-built software package which quantified the density of varicosities close to the surface of each myenteric cell body.
Results
UNASSIGNED
TH-immunoreactive varicosities had a greater mean density within 1 μm of the surface of ChAT +/NOS- nerve cell bodies compared with ChAT-/NOS + cell bodies. Similarly, ENK-immunoreactive varicosities also had a greater mean density close to ChAT +/NOS- cell bodies compared with ChAT-/NOS + cells.
Conclusion
UNASSIGNED
A method for quantifying close associations between varicosities and nerve cell bodies was developed. Sympathetic axons in the myenteric plexus preferentially target cholinergic excitatory cells compared to nitrergic neurons (which are largely inhibitory). This connectivity is likely to be involved in inhibitory modulation of human colonic motility by the sympathetic nervous system.
Identifiants
pubmed: 35368277
doi: 10.3389/fnins.2022.863662
pmc: PMC8970288
doi:
Types de publication
Journal Article
Langues
eng
Pagination
863662Informations de copyright
Copyright © 2022 Parker, Wiklendt, Humenick, Chen, Sia, Wattchow, Dinning and Brookes.
Déclaration de conflit d'intérêts
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Références
Z Zellforsch Mikrosk Anat. 1971;122(3):357-77
pubmed: 5120120
Neuroscience. 1983 Apr;8(4):653-64
pubmed: 6306502
J Comp Neurol. 1982 Feb 1;204(4):407-21
pubmed: 6277998
Neurogastroenterol Motil. 2016 Dec;28(12):1824-1835
pubmed: 27282132
J Chem Neuroanat. 2008 Dec;36(3-4):191-6
pubmed: 18572382
J Histochem Cytochem. 2014 Jul;62(7):519-31
pubmed: 24794148
Neurogastroenterol Motil. 2018 Mar;30(3):
pubmed: 28836741
Neurogastroenterol Motil. 2008 Dec;20(12):1298-305
pubmed: 18662329
J Pharmacol Exp Ther. 1965 Sep;149(3):358-64
pubmed: 4954685
J Comp Neurol. 1987 May 8;259(2):193-210
pubmed: 3584557
J Auton Nerv Syst. 1991 Jan;32(1):1-11
pubmed: 1673695
Clin Gastroenterol Hepatol. 2003 Mar;1(2):71-80
pubmed: 15017498
Cell Tissue Res. 2009 Oct;338(1):37-51
pubmed: 19711100
Anat Rec (Hoboken). 2012 Aug;295(8):1321-6
pubmed: 22678779
Nature. 1974 Aug 2;250(465):430-1
pubmed: 4853760
Histochem Cell Biol. 2005 Feb;123(2):131-8
pubmed: 15776249
Neurogastroenterol Motil. 2021 Jan;33(1):e13964
pubmed: 32839997
Br J Pharmacol. 2002 Feb;135(3):697-704
pubmed: 11834617
J Neurocytol. 1984 Feb;13(1):49-71
pubmed: 6707713
Br J Pharmacol. 1978 Oct;64(2):293-300
pubmed: 30507
J Physiol. 2001 Jul 15;534(Pt. 2):465-78
pubmed: 11454964
Gastroenterology. 1984 Sep;87(3):513-29
pubmed: 6745604
Eur J Pharmacol. 1970 Jan;9(1):80-4
pubmed: 5434296
J Histochem Cytochem. 1971 Nov;19(11):676-81
pubmed: 5121868
Acta Physiol Scand Suppl. 1969;335:1-116
pubmed: 4315733
Cell Tissue Res. 1995 Jun;280(3):549-60
pubmed: 7606768
Acta Physiol Scand. 1969 Jan-Feb;75(1):176-86
pubmed: 5785140
Neurosci Lett. 1989 Jan 30;96(3):259-63
pubmed: 2566138
J Comp Neurol. 2003 Apr 21;459(1):90-111
pubmed: 12629668
Chin J Physiol. 1999 Dec 31;42(4):201-10
pubmed: 10707895
Neurogastroenterol Motil. 2010 Jan;22(1):7-18
pubmed: 19686308
Br J Pharmacol. 1969 May;36(1):1-17
pubmed: 5768109
Neurogastroenterol Motil. 2007 Feb;19(2):126-34
pubmed: 17244167
Ann Med. 1998 Apr;30(2):151-8
pubmed: 9667793
J Chem Neuroanat. 1997 Mar;12(3):151-64
pubmed: 9141647
J Physiol. 1973 May;231(1):29P-30P
pubmed: 4715358
Gut. 2002 Jul;51(1):70-5
pubmed: 12077095
Am J Physiol. 1979 Jun;236(6):E738-45
pubmed: 443427
Neurogastroenterol Motil. 2004 Oct;16 Suppl 2:54-60
pubmed: 15357852
Int J Neuropharmacol. 1964 Sep;3:379-82
pubmed: 14334869
Neurogastroenterol Motil. 2021 May;33(5):e14046
pubmed: 33252179