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
PY - 2021/8/10
Y1 - 2021/8/10
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.
KW - Enteric Nervous System
KW - propulsion
KW - GI tract
KW - excitatory neuromuscular inputs
KW - inhibitory neuromuscular inputs
KW - mice
UR - http://www.scopus.com/inward/record.url?scp=85112103068&partnerID=8YFLogxK
UR - http://purl.org/au-research/grants/NHMRC/1156416
UR - http://purl.org/au-research/grants/ARC/DP190103628
U2 - 10.1038/s42003-021-02485-4
DO - 10.1038/s42003-021-02485-4
M3 - Article
AN - SCOPUS:85112103068
SN - 2399-3642
VL - 4
JO - Communications Biology
JF - Communications Biology
M1 - 955
ER -