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Abstract

The present study was aimed at elucidating how pacemaker activity (plateau potentials) (mean frequency: 15.9 +/- 2.8 times min(-1)) from submucosal interstitial cells of Cajal (ICC-SM) control spontaneous contractions in the mouse proximal colon. Mechanical activities in the circular muscle direction showed high-frequency (mean frequency: 15.6 +/- 2.7 times min(-1)) and low-amplitude (mean amplitude: 0.01 +/- 0.005 g) (HFLA) rhythmic contractions. Simultaneous recordings of circular muscle mechanical activity and electrical activity from ICC-SM revealed that HFLA contractions were synchronized with plateau potentials (mean frequency: 15.9 +/- 2.8 times min(-1)). Although low-frequency (3.5 +/- 2.1 times min(-1)) and high-amplitude (0.12 +/- 0.03 g) (LFHA) contractions in both longitudinal and circular muscle directions were synchronized with burst of action potentials in both muscle cells, these LFHA contractions were not synchronous with plateau potentials. Intracellular Ca2+ release from the internal stores through IP3 receptors is not a major factor to generate both action potentials differently from plateau potentials. Neither tetrodotoxin nor atropine affected the plateau potentials. The results reveal that the pacemaker activity from ICC-SM drives only the spontaneous HFLA (one-tenth amplitude of the LFHA circular and longitudinal muscle contractions) circular muscle contractions without control by enteric nerves.

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A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract.

Jeremy K M Sanders (1996)

Electrical rhythmicity in gastrointestinal muscles has been studied for a century, but the pacemakers driving this phenomenon have been elusive. Anatomic studies suggest that interstitial cells of Cajal (ICC) may be pacemakers and conductors of electrical activity. ICC may also mediate neurotransmission from enteric neurons. Functional evaluations of ICC include the following. (1) Electrophysiology experiments on dissected muscle strips show that slow waves originate from specific sites. These pacemaker areas are populated by networks of ICC that make gap junctions with smooth muscle cells. Removal of pacemaker regions interferes with slow wave generation and propagation. (2) Chemicals that label ICC histochemically can damage ICC and abolish rhythmicity. (3) isolated ICC are spontaneously active, and several voltage-dependent ion channels, including a low-threshold Ca2+ conductance, are expressed. (4) ICC are innervated by enteric neurons, and they respond to neurotransmitters. ICC may produce nitric oxide and amplify inhibitory neurotransmission. (5) Some classes of ICC fall to develop in animals with mutations in c-kit or stem cell factor, the ligand for c-Kit receptors. Without ICC, electrical slow waves are absent. Many questions remain about the function of ICC, but modern technologies should now facilitate rapid progress toward determining the role of these cells in normal physiology and pathological conditions.

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Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders.

J.D. Huizinga, L Thuneberg, J-M Vanderwinden … (1997)

Interstitial cells of Cajal (ICCs) have recently been identified as the pacemaker cells for contractile activity of the gastrointestinal tract. These cells generate the electrical 'slow-wave' activity that determines the characteristic frequency of phasic contractions of the stomach, intestine and colon. Slow waves also determine the direction and velocity of propagation of peristaltic activity, in concert with the enteric nervous system. Characterization of receptors and ion channels in the ICC membrane is under way, and manipulation of slow-wave activity markedly alters movement of contents through the gut organs. Here Jan Huizinga, Lars Thuneberg, Jean-Marie Vanderwinden and Jüri Rumessen, suggest that, as ICCs are unique to the gut, they might be ideal targets for pharmacological intervention in gastrointestinal motility disorders, which are very common and costly.

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Interaction of two electrical pacemakers in muscularis of canine proximal colon.

T K Smith, Stephen J. B. Reed, Jeremy K M Sanders (1987)

Experiments were performed to determine the source of the 20 cycles/min electrical oscillation commonly seen in colonic electrical records, the influence of the 20 cycles/min rhythm on the circular and longitudinal muscle layers, and the interactions between the 20 cycles/min rhythm and slow waves in circular muscle cells. Cross-sectional muscle preparations of the canine proximal colon were used to allow impalement of cells at any point through the thickness of the muscularis. Intracellular recordings from circular muscle cells clearly showed the two characteristic pacemaker frequencies in the colon (6 cycles/min slow waves; 20 cycles/min oscillations). The 20 cycles/min oscillations were recorded from longitudinal and circular muscle cells. Their amplitudes were greatest at the myenteric border. In the longitudinal layer the 20 cycles/min events initiated action potentials; in circular muscle the 20 cycles/min events summed with slow waves. Simultaneous recordings from circular and longitudinal cells across the myenteric border demonstrated that events in the two layers were usually in phase, suggesting that the two layers are electrically coupled and are paced by a common pacemaker. The amplitude of the 20 cycles/min events decayed with distance from the myenteric border in both circular and longitudinal muscles. The data demonstrate that two discrete populations of pacemaker cells generate the spontaneous electrical activity in the colon. Both events appear to passively spread through the circular muscle. It is the summation of these events that appears to serve as the signal for excitation-contraction coupling in circular muscle.

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PubMed ID:: 15500519

DOI:: 10.1111/j.1365-2982.2004.00546.x

ScienceOpen disciplines: Chemistry

Keywords: Animals,Biological Clocks,physiology,Calcium,metabolism,Calcium Channels,Colon,cytology,Inositol 1,4,5-Trisphosphate Receptors,Intestinal Mucosa,Male,Membrane Potentials,Mice,Mice, Inbred BALB C,Microelectrodes,Muscle, Smooth,Organ Culture Techniques,Receptors, Cytoplasmic and Nuclear

Pacemaker activity from submucosal interstitial cells of Cajal drives high-frequency and low-amplitude circular muscle contractions in the mouse proximal colon.

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Most cited references 12

A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract.

Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders.

Interaction of two electrical pacemakers in muscularis of canine proximal colon.

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