Korean J Physiol Pharmacol.  2015 Nov;19(6):533-542. 10.4196/kjpp.2015.19.6.533.

Electrophysiological and Mechanical Characteristics in Human Ileal Motility: Recordings of Slow Waves Conductions and Contractions, In vitro

Affiliations
  • 1Department of Surgery, Seoul National University College of Medicine, Seoul 03080, Korea. kjparkmd@plaza.snu.ac.kr
  • 2Department of Surgery, Seoul National University Bundang Hospital, Seongnam 13620, Korea.
  • 3Healthcare Research Institute, Seoul National University Hospital Healthcare System Gangnam Center, Seoul 06236, Korea.
  • 4Department of Physiology, Seoul National University College of Medicine, Seoul 03080, Korea.
  • 5Department of Pathology, Seoul National University College of Medicine, Seoul 03080, Korea.

Abstract

Little human tissue data are available for slow waves and migrating motor complexes, which are the main components of small bowel motility. We investigated the electrophysiological and mechanical characteristics of human ileal motility, in vitro. Ileum was obtained from patients undergoing bowel resection. Electrophysiological microelectrode recordings for membrane potential changes and mechanical tension recordings for contraction from smooth muscle strips and ileal segments were performed. Drugs affecting the enteric nervous system were applied to measure the changes in activity. Slow waves were detected with a frequency of 9~10/min. There were no cross-sectional differences in resting membrane potential (RMP), amplitude or frequency between outer and inner circular muscle (CM), suggesting that electrical activities could be effectively transmitted from outer to inner CM. The presence of the interstitial cell of Cajal (ICC) at the linia septa was verified by immunohistochemistry. Contractions of strips and segments occurred at a frequency of 3~4/min and 1~2/min, respectively. The frequency, amplitude and area under the curve were similar between CM and LM. In segments, contractions of CM were associated with LM, but propagation varied with antegrade and retrograde directions. Atropine, NW-oxide-L-arginine, and sodium nitroprusside exhibited different effects on RMP and contractions. There were no cross-sectional differences with regard to the characteristics of slow waves in CM. The frequency of contractions in smooth muscle strips and ileal segments was lower than slow waves. The directions of propagation were diverse, indicating both mixing and transport functions of the ileum.

Keyword

Human; Ileum; Motility; Slow Wave; Smooth Muscle

MeSH Terms

Atropine
Enteric Nervous System
Humans*
Ileum
Immunohistochemistry
Membrane Potentials
Microelectrodes
Muscle, Smooth
Myoelectric Complex, Migrating
Nitroprusside
Atropine
Nitroprusside

Figure

  • Fig. 1 Electrophysiological recordings of the circular muscle of the human ileum. (A) A microelectrode (3 M KCL, 50~80 Ω resistance) was inserted in the outer CM (a) or inner CM (b) of human ileum pinned down to expose the entire layer (M, mucosa; SM, submucosa; CM, circular muscle; LM, longitudinal muscle; S, serosa). (B) The slow wave, including the resting membrane potential (RMP) (c), plateau amplitude (d), and upstroke amplitude (e), was detected by CM.

  • Fig. 2 Electrophysiological and mechanical recordings of ileal smooth muscles. (A) The slow waves of ileal smooth muscle were measured by electrophysiologic recordings of the outer (a) and inner CM (b). (B) The contraction of muscle strips measured by tension recordings of the CM (c) and LM (d). (C) The contractions of ileal segments measured by tension recordings at the proximal (e), mid (f), and distal CM (g) and LM (h).

  • Fig. 3 The propagation patterns of human ileal contractions. (A) Antegrade propagation (40.0%) was observed, with contractions propagating from the proximal to distal part of the ileum. LM contraction synchronously cooperated with CM contraction. The dotted lines are connected by the time sequence of contractions at each part of the muscle. The sequence of contractions is also demonstrated by numbers in the circle. (B) Retrograde propagation (25.8%) was observed with contractions propagating from the distal to proximal part of the ileum. (C) A mixed pattern (34.2%) was also observed, with antegrade and retrograde propagations developing alternatively. Consequently, the materials in the ileum could be placed at the initial position, after a set of contractions.

  • Fig. 4 Change in the membrane potential and muscle strip and segment tension of human ileum after the administration of atropine (1 µM). On electrophysiological recording, the frequency of waves was slightly decreased after admission of atropine and RMP was not changed (a). Muscle strip contraction was decreased by atropine treatment (b). Ileal segment contraction was also decreased after the administration of atropine (c). The arrow indicates the administration of atropine.

  • Fig. 5 The change in membrane potential and muscle strip and segment tension of human ileum after the administration of Nw-oxide-L-arginine (L-NA) (100 µM). On electrophysiological recording, RMP was elevated after perfusion of L-NA (a). The contraction of muscle strips was enhanced by L-NA (b). The contraction of muscle segments was also enhanced after L-NA administration (c). The arrow indicates the administration of L-NA.

  • Fig. 6 The change in membrane potential and muscle strip and segment tension of human ileum after the administration of sodium nitroprusside (SNP) (100 µM). On electrophysiological recording, RMP was decreased after the perfusion of SNP (a). The contraction of muscle strips was eliminated by SNP and recovered after the drug was washed out (b). The contraction of muscle segments was not detected after SNP and was recovered after wash-out (c). The single arrow indicates the administration of SNP, and the double arrow indicates the wash-out.

  • Fig. 7 Immunohistochemical staining of human ileum and colon. (A) In the small intestine, c-kit(+) ICC are abundant and located in the interspace between the bulk of the inner circular muscle. (B) In the large intestine, c-kit(+) ICC are sparse and scattered in the inner circular muscle fibers (A: ×200, B: ×200) (CM, black thick arrow; LM, black thin arrow; ICC-MY, red thick arrow; ICC-SEP, red thin arrow).


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