Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice

• Published in: Communications biology 2021-08, Vol.4 (1), p.955-955, Article 955
• Main Authors: Spencer, Nick J., Travis, Lee, Wiklendt, Lukasz, Costa, Marcello, Hibberd, Timothy J., Brookes, Simon J., Dinning, Phil, Hu, Hongzhen, Wattchow, David A., Sorensen, Julian
• Format: Article
• Language: English
• Subjects: 631/378/1959; 631/378/3920; 64/60; 9/30; Animals; Biology; Biomedical and Life Sciences; Colon; Colon - innervation; Colon - physiology; Enteric nervous system; Enteric Nervous System - physiology; Female; Gastrointestinal tract; Large intestine; Life Sciences; Lymphatic system; Male; Mice; Mice, Inbred C57BL; Muscle contraction; Muscle Contraction - physiology; Muscle, Smooth - innervation; Muscle, Smooth - physiology; Nervous system; Portal vein; Smooth muscle; Synchronization
• ISSN: 2399-3642; 2399-3642
• DOI: 10.1038/s42003-021-02485-4

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. Nick Spencer et al. made simultaneous multi-site electrophysiological recordings with video imaging of colonic wall movements from ex vivo mouse colon, in order to correlate propulsion of content with underlying electrical signals from the smooth muscle. Their results demonstrate that excitatory and inhibitory junction potentials are synchronized in both the proximal and distal colon, suggesting that the enteric nervous system network communicates over a longer range than previously expected.