Abstract
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.
Highlights
How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue
Before the distension-evoked contraction was elicited in the proximal colon, a repetitive discharge of excitatory junction potentials (EJPs) was recorded in the smooth muscle of the mid colon at 1.57 ± 0.36 Hz (range: 1.2–1.9 Hz; N = 13; measured by Continuous Wavelet Transform (CWT) with a Morlet wavelet; See Fig. 1b, c and Supplementary Movie 1)
This is further exemplified in Supplementary Movie 2, which shows an expanded period of Supplementary Movie 1, with EJPs occurring at the same rates, with similar amplitudes and time courses, at both electrodes
Summary
How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. 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. 1234567890():,; In vertebrates, many hollow organs consist of layers of smooth muscle cells, which are rhythmically excitable and can generate propagating contractions that propel fluid over some distance. These include lymphatic vessels[1], ureters[2], urethra[3], some blood vessels[4] including the portal vein[5] and parts of the gastrointestinal (GI) tract[6]. Perhaps the major unresolved issue that has prevailed is how all these different classes of neurons in the ENS are temporally and spatially activated during patterns of motor activity that underlie propulsion along the gut
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