TY - JOUR
T1 - Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice
AU - Spencer, Nick J.
AU - Travis, Lee
AU - Wiklendt, Lukasz
AU - Costa, Marcello
AU - Hibberd, Timothy J.
AU - Brookes, Simon J.
AU - Dinning, Phil
AU - Hu, Hongzhen
AU - Wattchow, David A.
AU - Sorensen, Julian
N1 - Funding Information:
Experiments in this study were supported by an NHMRC Project grant #1156416 to N.J.S. & Australian Research Council (ARC) grant #DP190103628 to N.J.S. We are deeply grateful to Dr. David Wattchow for his generous support to purchase extracellular amplifiers used in this study. We thank the SA Biomedical Engineering, Research and Teaching Team for supporting this project through the development and construction of heated bases, faraday cages and organ baths used in this study.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. We reveal a mechanism that explains how ENS activity underlies propulsion of content along the colon. We used a recently developed high-resolution video imaging approach with concurrent electrophysiological recordings from smooth muscle, during fluid propulsion. Recordings showed pulsatile firing of excitatory and inhibitory neuromuscular inputs not only in proximal colon, but also distal colon, long before the propagating contraction invades the distal region. During propulsion, wavelet analysis revealed increased coherence at ~2 Hz over large distances between the proximal and distal regions. Therefore, during propulsion, synchronous firing of descending inhibitory nerve pathways over long ranges aborally acts to suppress smooth muscle from contracting, counteracting the excitatory nerve pathways over this same region of colon. This delays muscle contraction downstream, ahead of the advancing contraction. The mechanism identified is more complex than expected and vastly different from fluid propulsion along other hollow smooth muscle organs; like lymphatic vessels, portal vein, or ureters, that evolved without intrinsic neurons.
AB - How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. We reveal a mechanism that explains how ENS activity underlies propulsion of content along the colon. We used a recently developed high-resolution video imaging approach with concurrent electrophysiological recordings from smooth muscle, during fluid propulsion. Recordings showed pulsatile firing of excitatory and inhibitory neuromuscular inputs not only in proximal colon, but also distal colon, long before the propagating contraction invades the distal region. During propulsion, wavelet analysis revealed increased coherence at ~2 Hz over large distances between the proximal and distal regions. Therefore, during propulsion, synchronous firing of descending inhibitory nerve pathways over long ranges aborally acts to suppress smooth muscle from contracting, counteracting the excitatory nerve pathways over this same region of colon. This delays muscle contraction downstream, ahead of the advancing contraction. The mechanism identified is more complex than expected and vastly different from fluid propulsion along other hollow smooth muscle organs; like lymphatic vessels, portal vein, or ureters, that evolved without intrinsic neurons.
UR - http://www.scopus.com/inward/record.url?scp=85112103068&partnerID=8YFLogxK
U2 - 10.1038/s42003-021-02485-4
DO - 10.1038/s42003-021-02485-4
M3 - Article
C2 - 34376798
AN - SCOPUS:85112103068
SN - 2399-3642
VL - 4
JO - Communications Biology
JF - Communications Biology
IS - 1
M1 - 955
ER -