J. Physiol. (1972), 227, pp. 611-625 611With 6 text-ftguresPrinted in Great Britain

THE PROPAGATION OF SEGMENTAL CONTRACTIONSALONG THE SMALL INTESTINE*

BY M-L. GRIVEL AND Y. RUCKEBUSCHFrom the Laboratoire de Physiologie-Pharmacodynamie, Ecole

National Veterinaire, 31-Toulouse-03, France

(Received 10 July 1972)

SUMMARY

1. The electrical activity of the small intestine of conscious dogs,rabbits and sheep was recorded by means of chronically implanted elec-trodes and was related to mechanical changes in the bowel.

2. A pattern of activity characteristic of segmental contractions (aprolonged series of bursts of spike activity superimposed on the basicelectrical rhythm) was recorded successively at consecutive sites along thesmall intestine. This activity was as pronounced in the rabbits and sheepwhich were fed ad lib. as in the dogs which were fasted for 12 hr.

3. The segmental contractions began in the duodenum and had a fre-quency of 15-20/24 hr. As they passed along the intestine, their velocitydiminished and in the rabbits and sheep this was associated with anincreased duration of activity. Most of the contractions reached theterminal ileum taking 1 5-2 hr in each of the species despite the differencesin the length of the small intestine.

4. The propagation of segmental contractions appears to be a normaland common activity of the intact bowel and it may have a propulsiveas well as a mixing function.

INTRODUCTION

As early as 1869, Legros & Onimus noted the occurrence of rhythmiccontractions in the upper and lower segments of the small intestine in thedog. In 1902, Cannon described the character of these rhythmic con-tractions over a length of barium-filled bowel in both dogs and cats asstationary and restricted to a small area.However, according to Hukuhara (1930-1), motion pictures taken

through an 'abdominal window' in the dog show an unmistakable tend-ency of these contractions to move the digesta. In their detailed study ofthe contractions of exteriorized loops of the small intestine of the dog,

* The experiments described in this paper were performed in France.20-2

M-L. GRIVEL AND Y. RUCKEBUSCH

Douglas & Mann (1930) also noted a type of progressive segmentalcontraction with a number of segments contracting in a serial fashionin an aboral direction. Using tiny water-filled balloons arranged in tandemin fistulated dogs, Smith (1959) observed that relatively few segmentalcontractions of the duodenum occur simultaneously and that they occurmore often in an aboral sequence.

Alvarez & Mahoney (1922) were the first to identify the slow waveswhich recur at the same rate as the rhythmic segmental contractions. Sincethen, Bass & Wiley (1965) have demonstrated that the bursts of spikepotentials superimposed on the slow waves are chiefly related to contrac-tions of the circular muscle. Szurszewski (1969) observed a 'migratingelectric complex' along the small intestine of fasting dogs and suggestedthat this was probably associated with 'a caudally migrating band ofsegmental contractions'. Recently Carlson, Bedi & Code (1972) have shownthat this migrating activity can be propagated through isolated intestinalloops. Grivel (1971) has shown that a similar phenomenon occurs also inrabbits and sheep on a normal regimen.The work reported here shows that the migration of segmental contrac-

tions from duodenum to ileum is a normal process which occurs regularly indogs, rabbits and sheep at a velocity related to the length of the smallintestine. Techniques have been used which permit the electrical activityassociated with segmental contraction to be recorded in conscious animalsduring many weeks with minimal disturbance.

METHODS

Animal preparation. Measurements of the propagation of segmental contractionswere obtained from three dogs, three rabbits, and three sheep. The dogs weighed from15 to 20 kg, the rabbits from 2-5 to 3 kg and the sheep from 38 to 42 kg. Intestinalelectrodes were inserted into the animals under thiopentone anaesthesia with fullaseptic precautions. The electrodes were made from insulated nichrome wire, 120 #umin diameter and 50-100 cm in length (Ruckebusch, 1970). The insulation was burnedfrom the wire near to the tip and the end of the wire was inserted through the serosaand muscular layers, using a curved needle as a trocar; the free end was then tiedoff close to the intestine wall (see Fig. 1A). Insulation and fixation was achieved byproliferation of the serosa in approximately 4 days. Pairs of electrodes 2 mm apartwere positioned at right angles to the long axis of the bowel. Nine to twelve suchpairs were placed at equal or nearly equal intervals, the first pair being located 5 cmbeyond the pylorus and the last on the ileum at 20-40 cm from the caecum. Depend-ing on the length of the gut, the electrodes were 20-40 cm apart in the dog and therabbit and approximately 200-250 cm apart in the sheep.

Observations were made on animals placed in modified metabolism cages whichallowed them free movement but ensured sufficient restraint for long-term recordingtechniques. Rabbits and sheep were given hay ad lib. Dogs received one meal afterthe recording session, usually at 6.00 p.m. each day.

Record analy8i8. Recordings of the activity of the gut began 5 days after surgicaloperation and continued periodically for 6 weeks. They were obtained by use of a

612

SEGMENTAL CONTRACTIONS 613

direct writing polygraph (Reega VII, Alvar R.C. coupling, time constant 041 sec).A slow paper speed (2.5 mm/sec) was used for a minimum of 6 hr per day. Thepolygraph was connected to a magnetic tape recorder (Ana-Log 7, Phillips) toallow the records to be replayed at different speeds; replay at very high speeds wasespecially useful for displaying segmental contractions, as this form of activitydevelops gradually and recurs only at intervals of hours (see Fig. 5).

A _B

A; X in..;

v ..*. v)

1

2

Fig. 1. Implantation of electrodes, balloons, strain gauges and impedancebridges. In A, the free end ofan electrode is inserted through a curved needle(1); the insulated part of the electrode is tied off close to the intestinalwall (2) (dog, sheep and rabbit). The non-insulated part of the electrode isindicated by arrows. In B, a small balloon is held in place by two interruptedsilk sutures under an electrode site (dog and rabbit). In C, a strain-gaugewith a pair of electrodes attached is placed 10 cm proximal to a T-shapedcannula and the plates ofan impedance bridge are placed 10 cm distal (aboral)to the cannula (dog and sheep). The arrows indicate the direction ofdigesta flow.

The duration of activity at each electrode site was determined by direct inspectionof the record and the velocity of propagation was calculated from the time thatelapsed between the onset of activity at consecutive sites. The distance betweenelectrodes was noted at the time of the operation and was checked again at necropsy,where we found a 7-10% increase in intestinal length, and the mean value was usedfor calculations. Segmental contractions which did not propagate over the entirelength of the small intestine were excluded from these calculations. Observationsmade on other subjects with additional electrodes, on sheep with Thiry-Vella loopsand on dogs 1 month after reversal of a duodenal segment 10 cm in length arementioned as points of added interest.

Relationship between electrical and mechanical activity. Five days after chronicimplantation of electrodes on the duodenum of two other dogs and three rabbits,these animals were re-anaesthetized and movements of the duodenal wall were

M-L. GRIVEL AND Y. RUCKEBUSCHcarefully examined through a moist film of cellophane. A small water-filled balloon(0-2-0-8 ml.) was then positioned under one of the electrode sites, approachedfrom an aboral direction. It was attached at both ends to the intestinal wall above(see Fig. 1 B) using interrupted silk sutures. The pressure was recorded by aStatham transducer concurrently with electrical activity whilst the animal wasanaesthetized and again 2 or 3 days afterwards.

Additional dogs, rabbits and sheep were fitted with T-shaped cannulae in thedistal duodenum (see Fig. 1C). When the cannula was opened, the flow of digestacould be recorded by weighing the amount of fluid escaping at regular intervals. Astrain-gauge constructed on an appropriate frame was attached 10 cm proximal tothe cannula, one end being held against the mesenteric border with silk and the otheragainst the intestinal wall by the ends of the electrodes. Two stainless-steel plates(0.25 Cm2) mounted on a split sleeve of medical silastic were placed opposite oneanother 10 cm posterior to the cannula to detect by the impedance changes at ahigh frequency current (10 MHz) the variations in the diameter of the intestinallumen (Geddes & Hoff, 1964). This preparation was also provided with electrodesplaced near to the impedance bridge and near to the strain-gauge.

RESULTS

Types of electrical activity in the intestine. Two main types of electricalactivity (slow waves, corresponding to the basic electrical rhythm of theintestine, and spike potentials) can readily be distinguished in recordingsobtained from intestinal electrodes. Distinctions in the conscious animalcan be made between the following types of spike activity.

(i) Randomly occurring small bursts of spike potentials superimposedon the slow waves. This pattern of activity is associated with irregularand small movements of the intestine.

(ii) Groups of three or four strong bursts of spike potentials superim-posed on consecutive slow waves. They are propagated rapidly betweentwo or three sets of electrodes and are accompanied by peristaltic wavesof contraction at the same velocity.

(iii) Regular bursts of spike potentials superimposed on slow waves andlasting for some 3-9 min at any one site. The frequency of these burstscorresponds to the rate of segmental contractions which may also berecorded as well defined and simultaneous mechanical events. They areoften propagated over the entire length of the small intestine. Sometimessuch segmental contractions give rise to a peristaltic wave.

Interrelation of electrical and mechanical activity. After insertion of theintestinal balloon in anaesthetized animals, the movements of the intestinewhich could be observed by eye were related to the pressure changesrecorded by the balloon. This revealed some differences between dogs andrabbits. Fig. 2A shows that the pressure changes which are detected whenonly slow waves and weak and irregular spike activity are recorded werevery small in dogs, and no movement of the wall could be observedvisually. On the contrary some regular oscillations of the pressure in the

614

<SEGMENTAL CONTRACTIONS

balloon were seen at the same rate as that of the slow waves in rabbitsand were related to small but visible longitudinal movements of the wallover the balloon. When a burst of large spike potentials occurred in dogs,as in rabbits, a crease of the wall was seen and the pressure in the balloonrose sharply. As illustrated in Fig. 2B the greater the burst the greaterthe increase in pressure. In the dog the intestine appeared to relax fully

A Dog Rabbit

AJ\I I I.

6 sec 6 sec

Fig. 2. Relationship of electrical activity to pressure changes in the duo-denum. Spike activity was recorded by electrodes placed over a smallballoon fixed to the intestinal wall. Time scale: 6 sec, amplitude 100 1Wand 10 mm Hg. In A, in the dog regular pressure changes are recordedwith each burst of spike activity but not when spike activity is absent orirregular. In the rabbit regular oscillations of pressure are seen eventhough there is no spike activity. In B, the pressure changes are relatedto the intensity of the bursts of spike potentials.

between bursts of spike activity but in the rabbit a partial fusion of succes-sive contractions was often seen. Typical segmental contractions were notobserved in these anaesthetized preparations, but after recovery regularpressure changes lasting a few minutes were accompanied by regularbursts of spike potentials.

Table 1 shows the relationship between the magnitude and duration ofthe bursts of spike potentials and the strength of. contraction duringsegmental activity in conscious animals, 3 weeks after surgery. Whenmany spikes were recorded with each burst of activity, the decrease of thelumen diameter indicated by the impedance bridge correlated well withthe number of spikes for each burst of activity. The number of spike

615

M-L. GRIVEL AND Y. RUCKEBUSCHpotentials also showed a strong positive relationship with the extraluminalcontractile force recorded by the strain-gauges in sheep and dogs but thisrelation was less close in rabbits. These relationships are illustrated for thedog in Fig. 3. At the beginning of each of the segmental contractions,when there were few or no spikes superimposed on each slow wave, slightmechanical responses to the slow wave alone were observed in the dog andrabbit (as seen in the last row of values for each species in Table 1). Thesewere not evident in the sheep.

TABLE 1. The relation between number of spikes and the duration andmechanical correlates of spike activity during segmental contractions

Change inSpikes Duration of Contractile diameter*

Slow per the burst force* (impedancewaves slow (sec) (strain-gauge) bridge)

Species measured wave (mean value + S.D.)

Dog no. 3 17 7 0.87 + 0.05 4-00± 050 1.40 ± 0.3013 6 0-87 + 0-02 3.80± 040 1.04 + 0-1721 4 0-30+0.07 2t10±0.32 0-52±0*183 0 1.08+0.17 0

tCorrelationcoefficient (r) 0 94 0 97 0.99

Rabbit no. 2 22 18 0.90+0.10 3.70+0-17 1.14+0.1416 14 0-87 + 0-15 2-19 ± 014 0.83 0-1614 8 0-42 +0±06 0 94 + 0.20 037+ 0-147 0 0*31 + 0-16 0-27 0-08

tCorrelationcoefficient (r) 0-94 0-90 0.99

Sheep no. 2 32 16 0-67 + 021 2-60 + 0 40 2-10± 01030 12 0-56+0-15 2-05+0-17 1.90+0-1630 8 0-52+0-12 1-40+0-24 0 90+0.1420 0-4 0-21±0-06 0 0

tCorrelationcoefficient (r) 0Q96 0.99 0 93

* Indicated by the area in cm2 described by the polygraph pen at a speed of15 nmu/sec with a deflexion of one cm for 10 g on the gauge and 4 mm of reduction indiameter.

t Correlation with spikes significant at P < 0 05 in all instances.

During segmental contractions of the duodenum and jejunum theresponse of a strain-gauge aligned with the circular muscle layer and thenarrowing of intestinal diameter registered by the impedance bridgeindicate that a powerful contraction of the circular muscle is responsiblefor the majority of the spike activity that is recorded. The bursts of spikepotentials at one electrode site were characterized by their progressiveincrease in duration and their regularity for a few minutes (see Fig. 4).

616

SEGMENTAL CONTRACTIONS

Segmental contractions appeared to have a propulsive function in the con-tinuously fed sheep and rabbits. When such contractions were registered10 cm orally to a cannula, intestinal contents flowed slowly from the cannula,up to 40 ml. being expelled in the sheep for each period of contractionand one tenth of this volume in the rabbit. The flow ceased entirely for7-10 min after each period of contraction. Almost no flow of contentsoccurred during segmental contractions in the fasted dogs. A period of

A

3 sec 1 sec

B

2

Fig. 3. Relationship of electrical activity to extraluminal contractile forceand impedance changes in the duodenum of the dog. Recordings wereobtained from pairs of electrodes placed under the strain-gauge and close tothe impedance bridge. Calibrations: 10 g and 4 mm. In A, the forcerecorded by the strain-gauge (as indicated by the area described by a poly-graph pen) is related to the number of spikes in each burst. In B, a similarrelationship is evident between the number of spikes and the reduction inintestinal lumen diameter as recorded from the impedance bridge.

randomly occurring activity sometimes preceded this phenomenon,particularly in rabbits and sheep but also in dogs in the lower part of thesmall intestine. In this case, the associated pressure changes were not soprecisely related to spike activity. Segmental contractions may diminishprogressively and then may be followed by a propulsive wave as in Fig. 4 C.More frequently they ended abruptly and were followed by a long periodof quiescence during which no spiking activity occurred.The mean duration of the electrical activity differed between species

and parts of the small intestine (Table 2). The duration of discharge in-creased in the herbivores in the second half of the small intestine. Noconsistent change in the duration of segmental contractions was observed

617

M-L. GRIVEL AND Y. RUCKEBUSCH

when a recording session was prolonged beyond 24 hr. Segmental activityoccurred in sheep and rabbits regardless of their feeding time. In dogs,segmental contractions could not be distinguished for a period of 4 hrafter a meal.

A

_'~ b #t m ~

~~~~~~L t1. k- A LaA i I A. &AaAL aevA A A

C

&_LkniiA h Lk uUAL1

M V'" IF TTTI Ir Iri wrv -rr IrIr

30 sec

Fig. 4. Peristaltic waves and segmental contractions of the jejunum of thesheep. Recordings of the movements of the wall were obtained from astrain-gauge placed 5 cm caudally to the electrode site. Time scale: 30 sec,amplitude: 10 g and 100 #eV. In A, peristaltic waves are indicated by afew, strong bursts of spike potentials. In B, continuously rhythmic activityis related to segmental contractions. In C, a peristaltic wave starts at theend of a period of segmental contractions.

TABLE 2. Duration of segmental contractions (min, mean value + S.D.)20 days after implantation of electrodes

Position of electrodes(percentage of distance along total length of small intestine)

,~~~~~~~~A

Dogs 15% 30% 45% 90% 98%No. 1 (8)* 9-9+2-4 8-4+ 1-5 6-3+1-2 7-3+2-7 5-5+1-0No. 2 (8) 8-6 0-8 7-0 +0-7 6-7 +0-9 8-6 +1-8 6-5 ± 0-6No. 3 (8) 4-9+0-2 5-0+0-5 4-9+0-4 5-7+0-8 6-2+0-2Rabbits 20% 30% 45% 75% 95%No. 1 (12) 4-0+1-6 8-6+1-7 9-9±2-31 9-1+2-3 9-4+1-8No. 2 (9)- 6-3 +1-2 10-1 + 1-7 10-1+ 1-9 75 + 2-1No. 3 (12) 39 ± 0-8 7-0 +1-6 8-6 ± 1-7 99+ 2-3 9-4 + 1-8

Sheep 20% 30% 40% 50% 80%No. 1 (7) 3-2+1-8 3-9+1-1 5-3+0-9 4-9+1-7 -No. 2 (9) 3-2 0-8 5-7 +1-0 6-7 +1-2 7-1 + 0-9No. 3 (6) 5-1+0-7 5-9+0-8 6-22+0-9 6-9+0-7

* Indicates the number of observations.

618

SEGMENTAL CONTRACTIONS

Peristaltic contractions of the intestine could readily be distinguishedfrom segmental contractions (Fig. 4). The former consisted of a few burstsof spike potentials and associated increases in intraluminal pressure whichprogressed rapidly (8-15 cm/sec in the rabbit and sheep, 4-10 cm/secin the dog) between two sets of electrodes and resulted in the expulsion oflarge volumes of intestinal contents from an open cannula (10-40 ml. insheep, 2-5 ml. in both rabbit and dog). The segmental contractions were

signalled by regular bursts of spike potentials lasting a few minutes ateach electrode site. Such electrical activity thus appears to be an unmis-takable and convenient indication of segmental activity.

25 cm

65 cm

I I I

105 cm_ ,

145 cm

185 cm AL

0 8 16 24 32 40Time (min)

Fig. 5. Propagation of segmental contractions along the small intestine ofthe dog. The recordings were replayed from the magnetic tape at high speedso that only prolonged discharges were detected. Time scale in minutes.

Propagation of segmental contractions. In healthy subjects segmentalcontractions were always to be found at some point along the smallintestine, except for a few hours after feeding in the dog. Such activityoccurred at each recording site at approximately 90 min intervals. Exam-ination of the records from all electrode sites, played at high speed fromthe tape recorder (Fig. 5), indicates clearly that segmental activity waspropagated past each site in turn in an aboral direction.

619

M-L. GRIVEL AND Y. RUCKEBUSCH

The velocity at which segmental contractions passed from one site to thenext decreased with distance from the pylorus in each of the three species(Table 3). In the dog the velocity was 5-10 cm/min at the duodenal leveland only 1-2 cm/min in the ileum. As the mean duration time of seg-mental contractions was much the same at each site in the dog the lengthof the gut affected by segmental contractions in this species is shorter inthe lower part of the small intestine than in the duodenum. On the con-trary, similar calculations in the rabbit indicate that the length of small

TABLE 3. Mean velocity of propagation of segmental contractions (cm/min,mean value ± S.DA.) between consecutive electrode sites

Position of electrodes(percentage of distance along total length of small intestine)

Species ,Dogs 5-15% 15-30% 30-45 % 45-70% 70-90%No. 1. (8)* 8.9 + 3-5 5.7 +20 3.4 +13 2*3 +0-9 13 +0.2No. 2 (8) 5*1+0.7 6.8+1.5 5*7+1-4 2.2+002 1.3±0.1No. 3 (8) 5-8 + 1'7 5 0 + 12 4.8 ± 16 3.1 + 0-7 2.1 + 0 3

Rabbits 10-20% 30-45% 25-65% 65-85%No. 1 (2) 10.5+1-5 - 7*6+1X2 6.4+0±9 4'2+0±9No. 2 (9) 10-7±1.2 - 6.9+1-2 4-1+1 1 34+±1-0No. 3 (12) 7 9+0.7 6-7+0-9 5-1±0-9 4.1+009

Sheep 10-20% 20-30% 30-40% 40-50% 60-80%No. 1 (7) 88.0 ± 6.0 40-0 ± 2.0 37 0 +30 15-0+ 6-0 27-0 ± 3.0No. 2 (9) 116-0± 6-0 115-0+ 4-0 70 0 +20 69-0 +30 43-0 + 4 0No. 3 (6) 101-1+4-0 63.0+3±0 41-0±20 30-0+4-0 30.0+2±0

* Indicates the number of observations.

TABLE 4. Total time for segmental contractions to traverse the small intestine (inmin, mean value for six contractions ± S.D.) from 5 cm beyond the pylorus to 20 cmbefore the ileocaecal junction

Dogs Rabbits Sheep

No. 1 120+ 17-9 107+ 13-0 110+22.3No. 2 97 +14'6 102 + 16 4 103 +13.0No. 3 119 +19.2 86 ± 16 6 107 +18.2

intestine affected by segmental contractions increases with distance fromthe pylorus despite the reduced velocity. In the sheep, the velocity ofpropagation was about 10 times that seen in the rabbit yet the durationof activity at each site (Table 2) was only a little less. Thus, segmentalcontractions in the sheep must have involved a much longer length ofintestine than in the rabbit.The time necessary for segmental contractions to migrate from the first

620

SEGMENTAL CONTRACTIONSA. Dog

100 40 cm

50i14ILIso J. S ,Ia

_ I

l- - ..in. - l I

260cmi

1411 hr

B. Sheep

~~i~~hdI aid.~1Lh ij

I ~~~~~~~I I-~~~~~ 11 T

Fig. 6. Patterns of segmental activity in the dog and sheep. The percentageof slow waves on which bursts of spike activity were superimposed isplotted in black columns at 2 min intervals. Segmental activity was charac-terized by periods of maximal activity followed by periods of almostcomplete inactivity. In A, the four groups of electrodes are placed atdistances of 40 cm, 120 cm, 200 cm and 260 cm beyond the pylorus inthe dog. In B, the electrodes are placed at 2 m intervals in the sheep. Timescale in hours and periods of food intake between arrows.

u

621

M

l

M-L. GRIVEL AND Y. RUCKEBUSCHelectrode site 5 cm beyond the pylorus to the electrodes placed 20-40 cmfrom the ileo-caecal junction is approximately the same in each species,ranging only from 15-2 hr (Table 4). It was not always easy to measurethe velocity of propagation of the segmental activity with accuracy sincethe onset of this activity was usually gradual, especially in the ileum.Fig. 6 shows that the termination of segmental activity was much moresharply defined as segmentation was always succeeded by a period ofquiescence during which there was almost no spike activity.Not every segmental contraction was propagated over the full length of

the small intestine. Approximately one third of all the segmental contrac-tions observed disappeared after traversing 60% of the length of the smallintestine in the dog and 40% in the rabbit or sheep. Segmental contractionswere most likely to disappear in rabbits and in sheep after a sequenceof strong propulsive waves. Surgical interference with the intestine andchanges of diet also increased the proportion of segmental contractionswhich failed to be propagated.

Propagation across isolated or reversed segments of intestine. In sheepprepared with an isolated Thiry-Vella loop of intestine of 1 m length somesegmental contractions were seen to pass from the proximal intestine to theloop and then to return to the intestine beyond the site of anastomosis.When this happened the duration and velocity of segmental contractionspassing along the loop were similar to those on the intact intestine but thepropagation took 4-6 min to pass from the proximal part of the intestineto the loop and an equal time to pass from the loop to the distal part ofthe intestine. This delay at the transaction does not appear to be relatedto the reduced frequency of slow waves for although the latter occurredin dogs it was not seen in sheep or rabbits (Grivel & Ruckebusch, 1971).Only about 30 % of the segmental contractions seen on the intestineproximal to the loop passed to the loop and then back to the distal intes-tine in this manner. Some passed directly through the anastomosis withoutaffecting the loop. Other contractions ceased after a normal migration onto the loop. When surgical intervention resulted in excessive trauma allthe segmental contractions stopped at the anastomosis.

In the dog the propagation of segmental contractions may persist aftersection and reversal of a 10 cm length of the distal duodenum. A pair ofelectrodes inserted on each side of each anastomosis made it possible torecord the sequence of events due to segmental contractions. Despitea decrease in the frequency of slow waves on the segment and a delay inpassing the anastomoses, when slow waves on the duodenum proximalto the transaction line developed bursts of spike potentials, the slow wavesof the distal end of the reversed segment often also developed similaractivity. Subsequently, this activity progressed to the proximal end of the

622

SEGMENTAL CONTRACTIONSreversed segment and at last to the duodenum distal to the transaction.This phenomenon, and an increase in the frequency of the slow waves ofthe reversed segment when bursts of spike potentials occur on the duo-denum proximal to the transaction, are commonly observed from 20 daysto 2 months after surgery. A consistent but irregular reduction in theduration of the segmental contractions along the reversed segment wasalso noted and as in the sheep, with Thiry-Vella loops, more than 60%of the contractions did not pass the line of anastomosis.

DISCUSSION

The pattern of electrical activity associated with segmental contractionscan be identified without diffculty. There is no other activity which lastsas long as 3-9 min at a single electrode site. That segmental activity isso readily abolished by anaesthesia, surgical interference or changes indietary regimen means that it can be studied fully only in chronic prepara-tions. However, it is possible to observe directly in anaesthetized animals aclear relation between a burst of spike activity and a ring of contractionat the same level. This allows one to identify with confidence the electricalcorrelates of segmental contraction in the conscious animal. The motoractivity corresponding to segmental contractions in the animals fed ad lib.shows a slow increase in strength, followed by a long period of maintainedactivity which terminates abruptly. A long period of quiescence then occursas a sort of refractory period.The decrease of the diameter of the lumen detected by the impedance

bridge and the increased pressure in a balloon placed under an electrodesite show a positive correlation between the spike activity and the magni-tude of the contraction in the dog as well as in the sheep and rabbit,despite the existence of strong swaying (pendular) movements in the lastspecies. The absence of spike activity during visible contraction of thelongitudinal muscle suggests that this thin layer does not generate largenough potentials to be detected by extracellular electrodes in chronic

preparations. Possibly also the potentials are masked by those of thecircular muscle. For whatever reason, no spike potentials were recordedduring contraction of the longitudinal muscle, recognized in rabbits asoscillations of intraluminal pressure (Fig. 2A). The results given in Table 1support the opinion that most of the spike activity observed duringsegmental contractions originates in the circular muscle (Bass & Wiley,1965) but the experiments were not designed specifically to study thisquestion.Our experiments, like those of Code and his colleagues (Code, Szurszew-

ski, Kelly & Smith, 1968; Szurszewski, 1969; Carlson et al. 1972), show

623

M-L. GRIIVEL AND Y. RUCKEBUSCHclearly that segmental contractions are propagated, often over the wholelength of the small intestine. Our studies on three dissimilar species pro-vide the intriguing observation that the velocity of propagation (Table 3)is directly proportional to the length of the small intestine, so that ittakes the same time (about 1-52 hr) for the contraction to traverse theintestine in the dog or rabbit as it does in the sheep, despite the tenfolddifference in length. The gradual slowing of the wave of contraction as itpasses down the intestine occurs to a similar extent in the three animals,again despite the difference in length, and is associated with an increasedduration of activity in the sheep and rabbit.

Segmental contraction and peristaltic contraction both originate in theduodenum and occur there with a ratio that, in sheep at least, is related todiet (Ruckebusch, 1970). There is from an electromyographic point ofview little difference between the individual bursts of spikes seen duringperistaltic activity and those seen during segmental contractions. Thedifference between peristalsis and segmentation seems to lie mainly inthe speed at which the contraction wave moves down the intestine and inthe number of bursts of spike activity associated with each contraction -three or four rapidly propagated bursts in peristalsis and numerous burstsrecurring for periods of 3-9 min at successive sites in segmentation. Themechanisms underlying these differences remain uncertain. We suggest,however, that in each type of activity the velocity of propagation of theindividual burst of spikes is the same, that in peristalsis each burst ispropagated over long distances while in segmentation each burst is propa-gated for only a few cm before fading out and being replaced by the next.The experiments with isolated intestinal loops in sheep like those made

by Carlson et al. (1972) in the dog, indicate that neither the continuity ofthe bowel wall nor the presence of intestinal contents is needed for co-ordinated propagation of segmental activity. These experiments, togetherwith the study of the reversed intestinal segment in the dog, show thatthe activity is conducted orthodromically though it may sometimes eitherbe arrested at or jump directly across an intestinal anastomosis. In theserespects the propagation of spike activity of a segmental contractionwave resembles that of peristaltic waves, emphasizing again the basicsimilarity of the two sorts of activity.

Szurszewski (1969) has suggested that in the dog the segmental contrac-tions have the role of an 'interdigestive housekeeper', maintaining musclein condition and churning and propelling residual food and secretions.This role is fitting in the dog, in which the contractions occur only duringfasting, but does not adequately explain their function in more or lesscontinually feeding animals such as the sheep and rabbit in which segmen-tal contractions occur regularly in an intestine containing food. In these

624

SEGMENTAL CONTRACTIONSherbivores segmentation will certainly assist the mixing of food anddigestive secretions and encourage exposure of the mixture to the absorp-tive mucosa. The propulsive effect suggested by Code et at. (1968) fordogs appears to be more important in sheep and rabbits, judging by thevolumes of intestinal contents which were expelled through a cannula;however, one must view this result with caution since the presence of anopen cannula sets up an unnatural pressure gradient in an aboral direction.

The authors are grateful to R. N. B. Kay for discussion and criticism. Theyacknowledge financial support received from the C.N.R.S. (ERA no. 271).

REFERENCES

ALVAREZ, W. C. & MAHONEY, L. C. (1922). Action currents in stomach and intestine.Am. J. Physiol. 58, 476-493.

BASS, P. & WILEY, J. N. (1965). Electrical and extraluminal contractile forceactivity of the duodenum of the dog. Am. J. Dig. Dis. 10, 183-200.

CANNON, W. B. (1902). The movements of the intestines studied by means of theroentgen rays. Am. J. Physiol. 6, 251-277.

CARLSON, G., BEDI, B. S. & CODE, C. F. (1972). Mechanism of propagation ofintestinal interdigestive myoelectric complex. Am. J. Physiol. 222, 1027-1030.

CODE, C. F., SZURSZEWSxI, J. H., KELLY, K. A. & SMITH, I. B. (1968). A concept ofcontrol of gastrointestinal motility. In Handbook of Physiology: A Critical,Comprehensive Presentation of Physiological Knowledge and Concepts, section 6,vol. 5, pp. 2881-2896, ed. CODE, C. F. & HEIDEL, W. Washington D.C.: AmericanPhysiological Society.

DOUGLAS, D. M. & MANN, F. C. (1930). Experimental study of rhythmic contractionsin the small intestine of the dog. Am. J. Dig. Dis. 6, 318-322.

GEDDES, L. A. & HOFF, H. E. (1964). The measurement of physiological events byelectrical impedance. Am. J. med. Elect. 3, 16-27.

GRIVEL, M. L. (1971). Etude 6lectromyographique comparee de la motricite intesti-nale. These Doct. Sci. Nat., Toulouse, France.

GRIVEL, M. L. & RUCKEBUSCH, Y. (1971). A study in the dog and cat of the electricalactivity of the small intestine some months after transaction and transplantationof the gut. Life Sci., Oxford 10, 241-250.

HUxUHARA, T. (1930-1931). Die normale Dunndarmbewegung. Pfiugers Arch. ges.Physiol. 266, 518-542.

LEGROS & ONImuS (1869). Recherches experimentales sur les mouvements del'intestin. J. Anat. Physiol., Paris 6, 37-66.

RUCKEBUSCaH, Y. (1970). The electrical activity of the digestive tract of the sheepas an indication of the mechanical events in various regions. J. Physiol. 210,857-882.

SMITH, I. B. (1959). A study of small intestinal motility in dogs. Thesis, Universityof Cambridge.

SZURSZEWSKI, J. H. (1969). A migrating electrical complex of the canine smallintestine. Am. J. Physiol. 217, 1757-1763.

625