Spatial and temporal coupling between slow waves and pendular contractions
Wim J. E. P. Lammers
Department of Physiology, United Arab Emirates University, Al Ain, United Arab Emirates
Submitted 16 February 2005
; accepted in final form 11 July 2005
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ABSTRACT
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In contrast to the mechanisms of segmental and peristaltic contractions in the small intestine, not much is known about the mechanism of pendular contractions. High-resolution electrical and mechanical recordings were performed from isolated segments of the rabbit ileum during pendular contractions. The electrical activities were recorded with 32 extracellular electrodes while motility was assessed simultaneously by video tracking the displacements of 2040 serosal markers. The electrical activities consisted of slow waves, followed by spikes, that propagated in either the aboral or oral direction. The mechanical activity always followed the initial electrical activity, describing a contraction phase in one direction followed by a relaxation phase in the opposite direction. Pendular displacements were always in rhythm with the slow wave, whereas the direction of the displacements was dictated by the origin of the slow wave. If the slow wave propagated aborally, then the pendular displacement occurred in the oral direction, whereas if the slow wave propagated in the oral direction, then the displacement occurred in the aboral direction. In the case of more complex propagation patterns, such as in the area of pacemaking or collision, direction of displacements remained always opposite to the direction of the slow wave. In summary, the direction and pattern of propagation of the slow wave determine the rhythm and the direction of the pendular motility. The well-known variability in pendular movements is caused by the variability in the propagation of the underlying slow wave.
gastrointestinal motility; direction of propagation; electromechanical coupling; spikes
SEVERAL TYPES OF MOTOR PATTERNS have been investigated in the small intestine. Some of these, such as the peristaltic reflex, have been extensively studied, whereas others have not received that much attention. One type of behavior, referred to as "pendular contraction," "to-and-fro movements," or "sleeve contraction," (6, 20) has not been well described, although it has often been observed (14, 7, 11). Christensen (5), in an early review, sighed that "pendular movements are so poorly defined as to be incomprehensible."
There have been attempts to record pendular movements (3, 8, 10). Bayliss and Starling described the first tracings of the "pendulum" movements in dogs (1) and rabbits (2). Melville et al. (16) traced the longitudinal displacement of spots of India ink on the opposum duodenum. More recently, Hennig et al. (9) placed sutures onto the longitudinal coat of the guinea pig small intestine, video recorded their rhythmic contractions, and plotted them in spatial-temporal maps. Pendular contractions have even been modeled to show that they would mix luminal contents (15, 16). The major conclusion from these studies was that pendular movements were caused by contractions of the longitudinal muscle layer.
In the present study, we simultaneously recorded the electrical and mechanical activities of an isolated intestinal segment during pendular contractions and described in detail their spatial and temporal relationships. With this analysis, we show that the slow wave drives the pendular contraction and that the direction of slow wave propagation dictates the direction of the ensuing pendular movements.
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METHODS
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Mongrel rabbits (n = 14, 7 males and 7 females, average weight 1.2 ± 0.4 kg, mean ± SD) were used. The experimental procedure was approved by the Animal Research Ethical Committee, Faculty of Medicine and Health Sciences, of the United Arab Emirates University. After cervical dislocation, the abdomen was opened, and the small intestine was rapidly removed and placed in a dissecting dish containing cold Tyrode solution. A 10-cm-long segment of the ileum was dissected, gently flushed from the oral end, and transferred to a 250-ml organ bath. This custom-made tissue bath was made of Perspex sidewalls to allow a clear view for video recording. The preparations were superfused at a rate of 100 ml/min with a modified Tyrode solution [composed of (in mM) 130 NaCl, 4.5 KCl, 2.2 CaCl2, 0.6 MgCl2, 24.2 NaHCO3, 1.2 NaH2PO4, and 11 glucose] saturated with carbogen (95% O2-5% CO2) and kept at a constant pH (7.35 ± 0.05) and temperature (37 ± 0.5°C). The oral end of the tubular segment was connected to an infusion pump (Harvard Apparatus; 1 ml/min, infusion of Tyrode solution), whereas the distal end was attached to a short silicone tubing. The level of the outflow in the experiments was kept at the same level as the preparation to avoid distension of the preparation and initiate related contractions.
Electrical activities were recorded using a row of 32 extracellular electrodes (Teflon-coated silver wires, 0.3 mm diameter, 1 mm interelectrode distance). The tips of the electrodes were positioned as close as possible to the contracting muscle without actually touching it so as not to impede its movements. Recordings were made unipolarly with a large silver plate in the tissue bath acting as the indifferent pole. The electrodes were connected to 32 alternating current preamplifiers (gain 4,000), and the recorded signals were subsequently filtered (2400 Hz), digitized (8 bits, 1 kHz sampling rate/channel), multiplexed, and stored.
Soot markers (
2040) were placed on the serosal surface of the segment facing the video camera (13). A digital video camera (SONY DCR-TRV10E) was positioned against one of the Perspex sidewalls for a clear view of the tubular segment and its markers (Fig. 1A). Video recordings (25 frames/s, 720 x 480 pixels) were performed simultaneously with the electrical recordings for periods of 15 min. To synchronize the electrograms with the video signals, a digital stimulator (Neuro Data PG 4000) produced rhythmic pulses every 1 and 10 s, which were fed into one of the amplifiers and, converted in an auditory signal, recorded by the video camera. The resolution of the signals recorded in these experiments differ from each other; the electrical signals were sampled at 1 kHz (resolution of 1 ms), whereas the resolution of the motility signals was determined by the video frame rate (25 frames/s), resulting in a resolution of 40 ms.

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Fig. 1. A: diagram of the experimental setup with a 250-ml tissue bath, an isolated segment from the rabbit ileum, soot markers applied onto its surface, and a row of 32 extracellular electrodes along its length. A digital video camera, adjacent to the Perspex-walled tissue bath, recorded the spontaneous displacements of the markers. B: video snapshot of the preparation, showing the row of 32 electrodes and several soot markers. Twenty-six of those were identified (numbered crosses) and their displacements tracked.
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After the experiment, the electrical signals were analyzed using custom-made software (SmoothMap, written in Delphi) (14). For every slow wave cycle, the direction and pattern of slow wave propagation and, in the case of uniform propagation, the time difference between the first and the last slow wave recorded at opposite ends of the electrode array were measured. The displacement of the markers was analyzed using custom-developed software (MotilityMap, written in RealBasic 5.0; Fig. 1B) (13).
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RESULTS
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The spontaneous displacement of a single marker during pendular contraction is presented in Fig. 2. As shown in Fig. 2A, the majority of the displacements occurred in the longitudinal direction with very little movement in the circular direction. This is also evident when the displacements were plotted in time in the longitudinal direction, showing large excursions, and in the circular direction, demonstrating little change (Fig. 2B). In the longitudinal traces, the rhythmic displacements can be separated into three phases: 1) a resting phase, in which the tissue, after the previous contraction, moved back to its resting state; 2) a contraction phase, in which the markers displaced predominantly in the longitudinal direction; and 3) a relaxation phase, wherein the markers moved back.

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Fig. 2. Tracking and analyzing the displacements of the local markers. A: actual displacement of one marker during three successive cycles. The displacement occurred in a narrow loop with its major axis in the longitudinal direction. In B, this displacement was plotted against time in the longitudinal (top trace) and circular direction (bottom trace). Three phases are recognizable in the longitudinal displacement: a contraction phase and a relaxation phase followed by a period of rest.
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Pendular displacements occur in synchrony with the rhythm of the slow wave. This is shown in Fig. 3, where the slow wave propagated uniformly in the aboral direction. Figure 3, top, displays the 32 electrograms recorded during 3 successive slow wave cycles. The conduction time between the first and last recorded slow wave was 1.11.2 s (
2.7 cm/s). Figure 3, bottom, presents the displacements of 16 markers during this period. The markers all moved in the oral direction, in rhythm with the slow wave. The onset of the displacement was somewhat later than that of the slow wave, as evidenced by the three vertical lines. In addition, pendular motility also showed some phase differences because oral marker 1 started earlier than distal marker 16. The difference in time between these two markers ranged from 0.64 to 0.52 s.

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Fig. 3. Pendular displacements during aboral slow wave propagations. Top: 32 electrograms recorded along the length of an intestinal segment showing three successive slow waves (SW1SW3), propagating uniformly from oral to aboral followed, in many tracings, by numerous spikes. The slow wave propagation time from oral to aboral ranged from 1.10 to 1.21 s. Bottom: displacements of 16 markers that had occurred in rhythm with the slow waves. The locations of the original markers are depicted in the diagram to the left. Three vertical lines, drawn from the moment of the appearance of the first slow wave in lead 1 show that the displacements occurred after the initiation of the slow wave. The dashed arrows in the motility tracings represent the timing and direction of the slow waves superimposed on the motility tracings. The timing of the displacements in the first and last marker is indicated by the solid circles positioned halfway on the contractions. The displacements of the last marker occurred later than that of the first marker, although the time differences were less than those of the corresponding slow waves. In addition, the distal markers started to displace before the slow wave had actually reached that area (*).
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In the isolated intestine, spontaneous changes in pacemaker location and resulting direction of slow wave propagation often occur (14). Such events allowed us to analyze the ensuing patterns of pendular contractions. Figure 4 shows the situation in which the slow wave propagated in the oral direction. Three successive cycles are shown, with the electrical slow waves in Fig. 4, top, and the motility traces in Fig. 4, bottom. Again, there was synchrony between electrical activity and motility with the slow waves preceding the local displacements. The electrical slow wave propagated in the oral direction, and the local displacements occurred somewhat earlier at the distal than proximal end, while the differences in time are again smaller than that of the slow waves. The major difference between the motility traces during oral propagation compared with aboral propagation (Fig. 3) is that the markers displaced toward the distal part of the segment.

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Fig. 4. Pendular displacements during oral slow wave propagation. The presentation is similar to that in Fig. 3, with the electrograms (top) and simultaneously recorded displacements (bottom) shown. The vertical lines show that the slow waves preceded the displacements and that displacements in the distal end occurred earlier than those in the oral part of the segment. In contrast to the displacements shown in Fig. 3, the markers now displaced toward the aboral end of the preparation.
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This leads to a fundamental finding in this study. With pendular contractions, the tissue contracts first at the location from where the slow wave came from. This is due to the fact that the spikes, visible in the slow wave tracings in Figs. 3 and 4, occur immediately after the initiation of the slow wave. In the case of aboral propagation, the tissue will first be activated in the most oral part of the segment, and it is there that contraction will first occur. Because contraction induced a local shortening of the tissue, markers located further away will be pulled toward this initial site of contraction. As the slow waves propagated toward the distal end, spikes and local contraction followed, leading to the apparent propagation of motility as shown in the motility tracings. During propagation of the slow wave in the oral direction, this sequence of events occurred in the opposite direction, and the markers are then displaced toward the distal end, as shown in Fig. 4.
A consequence of the above is that if the tissue first contracted at one end, the other end must be initially stretched as both ends of the segment were fixed by their in- and outlets. This is shown in Fig. 5, in which the distance between neighboring pairs of markers was measured during the same cycles shown in Figs. 4 and 5. In the case of aboral propagation, at the proximal end, where the slow wave originated from, contraction occurred while the distal end was stretched. The opposite series of events occurred in the case of oral slow wave propagation (Fig. 5, bottom).

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Fig. 5. Local contractions and stretching during the aboral and oral slow wave propagations presented in Figs. 3 and 4. The distances between markers (average distance 5.5 mm; 3 of which are shown in the diagram in top and bottom) were plotted during 3 successive pendular contractions. The dashed arrows represent the timing and direction of the slow wave propagations during these events. The thin solid horizontal lines in each tracing indicate the resting distance between the markers. In the initial activated part of the segment, the distance between markers shortened, and hence local contraction occurred. These always occurred in the area where the slow wave had started, i.e., in the oral part during aboral propagation and in the distal part during oral propagation. At the other end of the segment, the distances between markers increased as the tissue was stretched due to contraction occurring at the other end. Areas located between these two extremes first showed stretch followed by contraction.
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Pendular contractions can become more complicated when other patterns of slow wave propagations occurred but are consistent with what was described with the previous uniform propagations. Figure 6 shows the situation in which a slow wave pacemaker was located in the middle of the segment, as shown during the first two slow wave cycles. The motility traces showed little displacements at the site of the pacemaker but increasingly larger displacements away from this site. Furthermore, the displacements occurred toward the area where the slow wave had originated. Therefore, both the oral markers and distal markers moved toward the center, in accordance with the rule presented earlier. The third cycle in this analysis happened to be an oral propagating slow wave with resulting displacements toward the distal end, similar to what was demonstrated before.

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Fig. 6. Patterns of electrical and motility activities when a slow wave pacemaker was located in the middle of the segment. The presentation is similar to that shown in Figs. 3 and 4. In the middle of the segment, where the slow wave originated from ( ), there is hardly any displacement, whereas their magnitude increased further away from the pacemaking site. Furthermore, the direction of the displacement was toward the origin of the slow wave as the oral and the distal markers displaced toward the center. In the third cycle, the pacemaker was located at the distal end, with subsequent oral propagation and concomitant distal displacement of the markers.
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The opposite pattern occurred when two slow waves propagated toward each other, colliding in the middle of the segment (Fig. 7). The motility traces shown in Fig. 7, bottom, now show displacements toward the oral end for the oral part and toward the distal end for the distal part of the preparation, again in accordance with the fact that pendular displacements occur toward the direction from where the slow wave came from. The middle part of the segment hardly displaced at all, as it was more or less simultaneously pulled from both ends.

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Fig. 7. Patterns of electrical and motility activities when two slow waves propagated toward each other and collided in the middle of the segment. Similar to the situation shown in Fig. 6, there is hardly any displacement in the middle of the segment, whereas maximal displacements occurred at the peripheries. In this case, however, markers are displaced toward the outer ends, to where the slow waves came from. In the third cycle, the pacemaker had shifted to the oral end, with subsequent aboral propagation and concomitant displacement of the markers toward the oral end.
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Pendular displacements are immediately affected by a change in direction of the slow wave. An example of this is shown in Fig. 8, in which a longer sequence of 12 slow waves and the resulting motility was analyzed. The dashed arrows, as before, were superimposed on the motility tracings, indicating timing and direction of the slow waves. Pendular displacements occurred toward the oral end with aboral slow wave propagation (Fig. 8, SW1 and SW12), whereas movements in the opposite direction occurred when the slow waves originated from the distal end (Fig. 8, SW7SW10). More subdued and complex motility patterns occurred in the case of pacemaking (Fig. 8, SW2SW6) and collision (Fig. 8, SW11). Changes in slow wave propagation are immediately reflected in changes in pendular displacements.

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Fig. 8. Spontaneous changes in slow wave direction are immediately reflected by changes in the direction of pendular contractions. In this 1-min recording, the slow wave pacemaker shifted spontaneously from oral to distal and back, as shown by the sequence of slow waves (top). Bottom: displacements reflect these variations in every cycle.
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The experimental situation is artificial in the sense that the segments could have been stretched by fixation to the in- and outlets. To determine whether this had any effect on the occurrence of pendular displacements, an additional five experiments were performed in which the suspended segments were stretched or compressed to various degrees. As shown in Fig. 9, pendular rhythm was present at the resting length of the segment (C), when it was stretched (D and E), and even when the tissue was compressed (A and B).

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Fig. 9. Pendular displacements during various degrees of stretch. Pendular displacements were recorded when the segment was kept at its initial length (C), stretched by 8% and 28% (D and E), or when the segment was compressed by moving the in- and outlets toward each other (A and B), thereby somewhat buckling the tissue. In all situations, pendular displacements and phase differences between various sites occurred, although the amplitude was higher and the displacements were slightly more regular when the preparation was stretched.
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DISCUSSION
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There is a close and causal relationship between the slow wave and the ensuing pendular displacements. Pendular motility is determined by the initial site of contraction, which in turn is determined by the origin of the slow wave. The coupling between slow waves and pendular displacements is performed by the action potentials (=spikes) that are initiated by the slow wave and that induced local contraction. Because the slow wave takes time to propagate and because spikes occur fairly quickly after the slow wave depolarization (17, 19), contraction in the segment will occur earlier at one end than at the other end. This asynchrony in contraction initiates displacement of the segment toward the area where the slow waves originated from and where the first spikes had occurred.
This relation between slow waves, spikes, contraction, and displacements is stable, as it holds under a variety of conditions as evidenced by spontaneous changes in the direction of propagation of the slow waves (Figs. 3, 4, and 68 ). Furthermore, the system does not seem to have a long memory as spontaneous and sudden changes in slow wave propagation were immediately reflected in changes in the direction of displacements of the markers. This was shown, for example, in the third cycles in Figs. 6 and 7 and more extensively in Fig. 8. Because pendular swings reflect the direction of the propagating slow wave, recording the direction of pendular swings could be useful in determining the direction of the slow waves.
The limitations of this study must be clear. This is not a detailed mapping study of the electrical propagation of the slow wave as presented earlier (14). This was not possible, as the electrodes would then have to be in contact with the preparation and thereby impede their movements. However, as shown in this study and in a previous one (12), it is possible to record local electrical activities with the electrode tips located at a short distance from the surface of the preparation, albeit at reduced amplitudes as is evidenced in the signals in the electrical records. Furthermore, the preparation is moving during the recording with respect to the position of the electrodes, making an accurate spatial determination of the slow wave propagation not possible. This was, therefore, not attempted. However, from the electrical signals, it is possible and permissible to determine the direction of propagation of the slow wave and to correlate that with the movement of each pendular contraction.
Other limitations relate to the in vitro nature of the study, the use of a single species, and, indeed, of one part of the small intestine.
Within these limitations, the conclusions are clear in that it is the direction of slow wave propagation that determines the direction of the pendular movements. It is therefore, in retrospect, no surprise that pendular contractions, in contrast to other types of contraction, were deemed to be "incomprehensible" (5). They do not show a stereotypical pattern such as the peristaltic reflex (18). Instead, pendular contractions and pendular movements are determined and controlled by the slow waves. Because slow wave origins and propagations are not fixed but show continuous and spontaneous changes (14), the ensuing pendular motility reflects this inherent variability.
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GRANTS
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This study was supported by the Faculty of Medicine and Health Sciences, United Arab Emirates University.
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ACKNOWLEDGMENTS
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The author acknowledges the work of D. Dhanasekaran, who constructed the tissue bath and the 32-electrode array, and B. Stephen for the experimental assistance. The slow wave and displacements tracings presented in Figs. 3, 4, and 68 are available as "pendular movies," which can be viewed and downloaded from www.smoothmap.org.
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FOOTNOTES
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Address for reprint requests and other correspondence: W. J. E. P. Lammers, Dept. of Physiology, Faculty of Medicine and Health Sciences, PO Box 17666, Al Ain, United Arab Emirates (e-mail: wlammers{at}smoothmap.org)
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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REFERENCES
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- Bayliss WM and Starling EH. The movements and innervation of the small intestine. J Physiol 24: 99143, 1899.
- Bayliss WM and Starling EH. The movements and innervation of the small intestine. J Physiol 26: 125138, 1901.
- Berkson J, Baldes EJ, and Alvarez WC. Electromyographic studies of the gastrointestinal tract. I. The correlation between mechanical movement and changes in electrical potential during rhythmic contraction of the intestine. Am J Physiol 102: 683- 692, 1932.[Free Full Text]
- Cannon WB. The Mechanical Factors of Digestion. Facsimile of the 1911 ed. Abingdon, UK: Oxford Historical Books, 1996.
- Christensen J. The controls of gastrointestinal movements: some old and new views. N Engl J Med 285: 8598, 1971.[ISI][Medline]
- Christensen J. Motility of the intestine. In: Gastrointestinal Disease (5th ed.), edited by Sleisenger MH and Fordtran JS. Philadelphia, PA: Saunders, 1973, vol 1, chapt 38, p.822837.
- Ehrlein HJ, Schemann M, and Siegle ML. Motor patterns of small intestine determined by closely spaced extraluminal transducers and videofluoroscopy. Am J Physiol Gastrointest Liver Physiol 253: G259G267, 1987.[Abstract/Free Full Text]
- Gonella J. Etude de l'activité électrique de la couche musculaire longitudinale du duodenum de lapin. J Physiol 62: 447476, 1970.
- Hennig GW, Costa M, Chen BN, and Brookes SJH. Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J Physiol 517: 575590, 1999.[Abstract/Free Full Text]
- Hukuhara T. Weitere studien über die normale Dünndarmbewegung. Pflügers Arch 235: 164175, 1934.
- Krishnan BT. Studies on the function of the intestinal musculature. I. The normal movements of the small intestine and the relations between the action of the longitudinal and circular muscle fibres in those movements. Q J Exp Physiol 22: 5763, 1932.
- Lammers WJEP, Arafat K, El-Kays A, and El-Sharkawy TY. Spatial and temporal variations in local spike propagation in the myometrium of the 17-day pregnant rat. Am J Physiol Cell Physiol 267: C1210C1223, 1994.[Abstract/Free Full Text]
- Lammers WJEP, Dhanasekaran S, Slack JR, and Stephen B. Two-dimensional high resolution motility mapping. Methodology and initial results. Neurogastroenterol Motil 13: 309323, 2001.[CrossRef][ISI][Medline]
- Lammers WJEP, Stephen B, Arafat K, and Manefield GW. High resolution mapping in the gastrointestinal system: initial results. Neurogastroenterol Motil 8: 207216, 1996.[ISI][Medline]
- Macagno EO. Fluid mechanics of the duodenum. Ann Rev Fluid Mech 12: 139158, 1980.[CrossRef][ISI]
- Melville J, Macagno E, and Christensen J. Longitudinal contractions in the duodenum; their fluid-mechanical function. Am J Physiol 228: 18871892, 1975.[Abstract/Free Full Text]
- Sancholuz AG, Croley TE II, Christensen J, Macagno EO, and Glover JR. Phase lock of electrical slow waves and spike burst in cat duodenum. Am J Physiol 229: 608612, 1975.[Abstract/Free Full Text]
- Schulze-Delrieu K. Visual parameters define the phase, and the load of contractions in isolated guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 276: G1417G1424, 1999.[Abstract/Free Full Text]
- Summers RW and Dusdieker NS. Patterns of spike burst spread and flow in the canine small intestine. Gastroenterology 81: 742750, 1981.[ISI][Medline]
- Thuneberg L and Peters S. Toward a concept of stretch-coupling in smooth muscle. I. Anatomy of intestinal segmentations and sleeve contractions. Anat Rec 262: 110124, 2001.[CrossRef][ISI][Medline]
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