Motility of the rabbit's colon and cecotrophy

Physiology & Behavior, Vol. 18, pp. 871-878. Pergamon Press and Brain Research Publ., 1977. Printed in the U.S.A.

Motility of the Rabbit's Colon and Cecotrophy Y. R U C K E B U S C H AND H. H O R N I C K E Labomtoire de Physiologie-Pharmacodynamie, Ecole Nationale V(;tdri~zaire. 23 chemi~l des Cal;elles 31076 TOulouse C~dex, France and (;)liversitdt Hohenheim, hTstitut fiir Zooplo, siologie, 7 Stuttgart 70 (F R. G.) (Received 9 April 1976)

RUCKEBUSCH Y. AND H. HORNICKE. MotiliO, of the rabbit's colon and cecotrophy. PHYSIOL. BHtAV. 18(5l 8 7 l - 8 7 8 , 1977. The characteristics of hard and soft (cecotroph) pellet production were investigated in rabbits led one 4 hr meal daily. Changes in colon motility related to feeding and cecotrophy (coprophagy) recorded by means of chronically implanted electrodes are described. The increased activity of the proximal colon observed during t'eeding is followed by an increase in the number of contractions propagated along the distal colon and emission of hard feces. The subsequent elimination of soft feces is preceded by a specific pattern of increased activity on the aboral part of the proximal colon which migrates towards the rectum (3 4 hr). The results suggest that the sequential changes in activity of different parts of the colon are the key to solving the enigma of the emission of soft feces: the elimination of hard feces from the dis~al colon triggering an increased activity orad to the fi~sus coil Electromyography

Colon

Cecotrophy

Rabbit

RUCKEBUSCH Y. ET H. HORN1CKk;. Motricitd colique et caecotrophie chez le lapin. PHYSIOl.. BI:HAV. 18(5) 871 878, 1977. La production de f~ces dures et f~ces molles (caecotrophes/ a ~td envisag~c chez le lapin recevant un repas quotidien de granules durant 4 heures. Les variations concomitantes de l'activit~ ~lectriquc de la paroi du c61on proximal et distal ont dtd enregistrdes fi partir d'61ectrodes laiss~es fi demeure. L'activitd dlectrique de la totalitd du c61on est accrue pendant le repas, lequel est suivi de l'~;mission de f~ces dures pendant 3 4 heures. La production dc caecotrophes est accompagn~e d'une pdriode d'hyperactivit6 du segment aboral du c61on proximal qui envahit cn 3 ~t 4 hcures la totalit~ du c61on distal; ce d~lai est celui au bout duquel apparaft l'dmission des caecotrophes. (>s rdsultats soulignent l'importance de l'ordre dans lequel apparaissent les modifications motrices des diffdrentes parties du c61on: la vacuit~ du c61on distal due fi l'dmission de fOces dures est fi l'origine de I'hyperactivit~ de la pattie du c(flon proxmlal responsable de la production de f~'ces molles: le ddplacement de cette zone d'hyperactivitd le long du c6[on distal s'acconrpagne de leur ~mission. I,ilectromyographie

CSlon

Caecotrophie

Lapin

THE RABBIT p r o d u c e s two kinds o f feces in a regular p a t t e r n : the e l i m i n a t i o n of hard pellets [171 being interrupted once or twice daily by the p r o d u c t i o n o f soft pellets or c e c o t r o p h s [ 1 4 , 1 9 ] . Reingestion of soft pellets in the rabbit and the hare [28] is t e r m e d c o p r o p h a g y [7] or m o r e precisely c e c o t r o p h y [ 2 6 ] . Both hard and soft feces originate from the same cecal material, the later having a higher water, e l e c t r o l y t e and n i t r o g e n c o n t e n t [ 4 , 9 ] . C e c o t r o p h y occurs at fixed intervals after the cecal hyperactivity which a c c o m p a n i e s , and persists for some time after, each daily meal [11, 22, 24, 2 5 ] . It c o n t i n u e s to occur after v a g o t o m y w h i c h abolishes the p o s t p r a n d i a l cecal response [ 2 4 ] . This behavior is an ingenious process which permits m a x i m a l g a s t r o d u o d e n a l a b s o r p t i o n o f valuable food substances.

As early as 1925, Auer suggested a role in scybala f o r m a t i o n for the spindle-shaped and thicker-walled fusus coli w h i c h separates the p r o x i m a l and distal colon [2]. lie n o t e d in a n e s t h e t i z e d rabbits that the scybala on the p r o x i m a l colon side were large, grayish, soft and rich in water, while those i m m e d i a t e l y below the /Usus coli were smaller grayish yellow, hard and dry. One p r o p o s e d e x p l a n a t i o n for the emission of soft pellets is a decrease of the activity o f the fusus coll. However m o r e c o m p l e x changes seem to be involved since p r o d u c t i o n o f soft pellets is still possible after surgery to bypass the .(~sus coli [231. thus eliminating a major role for this structure. A separation of the solid and liquid phases in the p r o x i m a l colon has r e c e n t l y been described [3] on the basis of radioscopic studios. They revealed a back-flow o f the liquid phase from 871

872

RUCKEB1 SCH ;kNI) H O R N I C K t

the proximal colon towards the cecum and preferentia~ cecal c o n c e n t r a t i o n of a liquid marker, giving rise lo the hypothesis that antiperistalsis [8] plays an i m p o r t a n t role in the differential f o r m a t i o n of pellets. These antiperistaltic contractions only involved the oral triple haustrated part of the proximal colon and not its aboral single haustrated part: these two regions show no changes in activity during the production of soft pellets which is suspected to occur from 2- 4 hr before defecation [ 1 2,18]. The purpose of the present study is (1) to provide a basic description of the m o t i l i t y of the large intestine in rabbits fed once daily, (2) to d e t e r m i n e the patterns of activity of the different parts of the colon, especially the aboral part of the proximal colon, in relation ~o lhe production and elimination of the two kinds of feces.

cecum and the different parts o: ~lic coto~ 1 2 4 j l h e anintals were housed in individual cages and periods o i c e c o t r o p h y were recorded by c(~r~;~nu~ts dJ~ect observ~t tion. I:lectrophysiological data were ~'cold~-d o n a 12 chmlnei polygraph (Alvar, Paris) at a papc~ ';peed of 2.5 ram/see over 24 hr periods *or 4 to 6 weeks c o m m e n c i n g 10 days after surgery. From time to time samples were taken al other speeds (15 and 30 mm/'seci. :iracings were visually scored in 2 min epochs, the presence of spike activity being expressed as a percentage of recording l m ~ t

R ESI.TI. I'S

Time Relationship Between Feeding and ( ecotroph3 METHOD

A mean daily food c o n s u m p t i o n o i 167 -+- 34 g in 2 5 - 3 5 meals was observed in the rabbits of G r o u p A with i'ree access to food. The ratio of time spent feeding during the day and night-light was 1:4. Hard feces 0 n e a n dry matter: 53%) were eliminated 10 -14 times per 24 hr mainly during the night-time. Soft feces p r o d u c t i o n (mean dry matter: 31%) in five of the animals started between 0 3 : 0 0 and 0 8 : 0 0 and persisted until 14:00 to 17:00 (Table 1~. When access to food was restricted to 4 hr per day the mean c o n s u m p t i o n was reduced by 49~);. Hard and soft feces p r o d u c t i o n was decreased by 22 and 50% r e s p e c t i v e l y A b o u t 80% of the hard feces were eliminated during the 4 hr postprandial period. The emission of soft feces then c o m m e n c e d , quickly reached a peak and persisted for 3 4 hr. The same time relationship b e t w e e n feeding and production of hard and soft pellets was found in all the animals (Fig. 1). Occasionally a second but shorter period of c e c o t r o p h y was recorded 4--5 hr after the end of the major emission.

Rabbits of b o t h sexes weighing 2.7 3.3 kg were used. The animals were collared and housed in individual cages fitted with a feeding box. Overhead lighting was automatically timed to a 1 2 hr l i g h t - d a r k cycle with lights on at 06:00. Group A comprised 3 males (Nos. 1, 2, 3) and 3 females (Nos. 4, 5, 6) fed a standard laboratory diet (mean dry m a t t e r 90%) ad lib and then had their food supply restricted to 4 hr daily ( 1 0 : 0 0 14:00). This later procedure was used to obtain predictable periods of hard and soft feces elimination. F o o d c o n s u m p t i o n was measured by weighing the animals. The hard and soft feces were collected either at hourly intervals from a continuously moving belt or by an a u t o m a t i c sampler t h r o u g h o u t 24 hr periods [15]. Group B comprised 6 females fed according to the same schedule and chronically implanted with paired electrodes [231 placed at fixed distances along the distal ileum, the

TABLE 1 FOOD INTAKE AND FECES PRODUCTION IN RABBITS OF GROUP A (MEAN VALUES FOR 5 DAYS) F e c e s (g)

Cecotrophy (h)

Food intake (g)

Hard

Soft

Duration

Onset

137 174 168 178

103 107 113 114

128 130 99 130

09-12 08-11 07-11 09-13

198 145 167 _+ 34

122 90 108 _+ 18

129 96

09-13 07-11

(kf4)6 05-07 06-08 23-02 & 01-05 04-08 & 06-09 03-06 06--08

ll9 - 23

9,5 _+ 1,0

99 104 78 62 85 86

100 97 80 60 64 102

68 43 78 49 44 72

06-08 06-07 08-10 07--09 07-09 08-l)9

86 + 16

84 + 20

59 + 18

8,0 _+ 1,0

Fed ad lib

n° I 2 3 4* 5 6 M e a n _ S.D. Fed from 10-14 hr

n° 1 2 3 4 5 6 M e a n -+ S . D .

* T w o c e c o t r o p h y periods during ad lib f e e d i n g w e r e regularly o b s e r v e d in Rabbit 4.

16--17 18---20 18--19 t 6-t 9 17-18 16-t7

C O L O N M O T I L I T Y AND C E C O T R O P H Y

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873

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Ascending cecal controchon initiating at t h e c e c o - c o l i c junction

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FIG. 1. Time relationship between the hourly production of hard and soft pellets in a rabbit fed once daily from 10:00 to 14:00.

Ascending cecal contraction following ontipenstalsJs on proximal colon

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5

Electrical A ctivitv o f the Cecum and Proximal Colon (Oral Part) During the interdigestive p e r i o d in r a b b i t s receiving one daily meal, the c o n t r a c t i o n of the cecal wall was characterized by s t r o n g b u r s t s of spike p o t e n t i a l s lasting 4 - 5 sec. The f r e q u e n c y of c o n t r a c t i o n s varied f r o m 0.5 to 1.2/rain and t h e y were rapidly p r o p a g a t e d e i t h e r from the base to the apex ( a s c e n d i n g c o n t r a c t i o n s ) or in the reverse d i r e c t i o n ( d e s c e n d i n g ) w i t h a m e a n r a t i o of the two t y p e s of 1.2:1. The f r e q u e n c y of slow waves o n the p r o x i m a l c o l o n was a b o u t 13.8 near the ceco-colic j u n c t i o n , 16.3/rain on the oral part a n d 17.3/rain on the a b o r a l part. A lower slow-wave f r e q u e n c y of 9/rain was also r e c o r d e d occasionally on the p r o x i m a l c o l o n near the j u n c t i o n , especially after the passage of a p r o l o n g e d b u r s t of spike potentials. The a m p u l l a cecalis colt did n o t e x h i b i t slow waves. Spiking activity o c c u r r e d e i t h e r as series of bursts, at the same f r e q u e n c y as the slow waves, lasting 10 to 60 sec or as a single p r o l o n g e d b u r s t of spike p o t e n t i a l s . These single p r o l o n g e d b u r s t s originated e i t h e r near the a m p u l l a cecalis and were p r o p a g a t e d t o w a r d s the colon, or m i d w a y along the p r o x i m a l colon and p r o p a g a t e d t o w a r d s the c e c u m lantiperistalsis). In b o t h cases, t h e y were associated with an a s c e n d i n g cecal c o n t r a c t i o n (Fig. 2). In a d d i t i o n , a f t e r a d e s c e n d i n g cecal c o n t r a c t i o n single p r o l o n g e d bursts of spike p o t e n t i a l s were r e c o r d e d o n the p r o x i m a l c o l o n (Fig. 2). F o r a 24 hr period, t h e m e a n ratio, b e t w e e n c o n t r a c tions of t h e p r o x i m a l c o l o n p r o p a g a t e d from the cecum, and c o n t r a c t i o n s p r o p a g a t e d t o w a r d s the c e c u m was 10:0.6 in animais fed ad lib and I 0 : 1 . 2 in t h o s e receiving one daily meal. The c o n t r a c t i o n s o f the p r o x i m a l colon w h i c h were n o t associated w i t h t h o s e of the c e c u m r e p r e s e n t e d 36% of all c o n t r a c t i o n s in animals receiving one daily meal (Table 2). Peristaltic c o n t r a c t i o n s on the p r o x i m a l c o l o n initiating at the ceco-colic j u n c t i o n s i m u l t a n e o u s l y with ascending cecal c o n t r a c t i o n s r e p r e s e n t e d 35 40% of the t o t a l n u m b e r of c o n t r a c t i o n s r e c o r d e d in r a b b i t s e i t h e r fed ad lib or one daily meal; ascending cecal c o n t r a c t i o n s following antiperistalsis on the oral part of the p r o x i m a l colon were less f r e q u e n t (6 10~Tc). The d e s c e n d i n g cecal c o n t r a c t i o n s propagated t h r o u g h the ceco-colic j u n c t i o n and f o l l o w e d by a peristaltic c o n t r a c t i o n of the c o l o n r e p r e s e n t e d 32% of the total in animals fed ad lib and only 18% in those receiving

I

Descending cecar contraction propagated through the ceco-colic junction

6

FIG. 2. Patterns of electrical activity recorded during tile interdigestive period in the rabbit receiving one daily meal. The pairs of electrodes were placed on the ceco-colic junction [4], at inlervals o[" 9 cm on the cecum [1, 2, 3] and 6 cm on the aboral part o t t h c proximal colon [5, 6, 71 with one pair ~q electrodes [81 ~)n the aboral part of the proximal colon at 10 cnl tram 7. Note a decrease by 5t)c,V in the slow-wave frequency (underlined) ~d" the colon [5 I seen after an ascending contraction on the cecum l'rom the ,itmclion (upper pane[) or through the junction from the proximal cohm (middle panel). This is not the case for descending cecal contraction through the junction dower paneI I.

one daily meal (Table 2). This r e d u c t i o n in the n u m b e r o f d e s c e n d i n g cecal c o n t r a c t i o n s p r o p a g a t e d t h r o u g h the ceco-colic j u n c t i o n in animals on a restricted feeding schedule seemed related to the r e d u c e d food i n t a k e and slower cecal e m p t y i n g . During feeding, the activity of the c e c u m and p r o x i m a l colon was strongly increased and r e m a i n e d so for long periods in animals fed ad lib. However d i s t i n c t i o n b e t w e e n c o n t r a c t i o n s restricted to e i t h e r cectm3 or colon (22% o f all c o n t r a c t i o n s ) and c o n t r a c t i o n s p r o p a g a t e d l h r o u g h the ceco-colic j u n c t i o n always r e m a i n e d clear (Fig. 3).

Electrical Activity o f the [leo-Ceco-Colic Junction The electrical activity of the ileum e x h i b i t e d slow waves

874

RUCKEBUS('It A N D f t 0 R N I C K [ ~. TABLE 2 NUMBER OF CONTRACTIONS OF THE CECUM AND OF "[HE PROXIMAL COLON IN 4 RABBII'S OF GROUP B IMEAN VALUES FOR DAYS, -

Cecal contractions 08:00-20:00 20:00-08:00

Contractions of the proximal colon (%) Isolated from Associated with cecal cecal contraction contractions Ascending Descending

Fed ad lib Mean S.D.

973 47

776 70

21 7 8.7

39.5~- 6.25 4.8 2.3

32.7 65:

Fed from 10-14 hr Mean S.D.

618" 66

862 93

36.0* 6.2

35.8 4.4

18.0" 2_-

10.2 2.7

*p<0.01--Ascending cecal contractions: "~initiating at the cecocolic junction: and ~:foltowing antiperistalsis the proximal colon. at a m e a n f r e q u e n c y of 15.3/rain ~11.5 17.5~ w i t h s u p e r i m p o s e d b u r s t s o f spike p o t e n t i a l s o f 200 uV amplit u d e lasting 2 - 3 sec a n d o c c u r r i n g at the same r h y t h m . In c o n t r a s t , o n l y isolated b u r s t s of spike p o t e n t i a l s of 500 , V a m p l i t u d e lasting 4 - 5 sec were r e c o r d e d on the sacculus r o t o n d u s . D e s c e n d i n g c o n t r a c t i o n s of the c e c u m a c t i v a t e d the sacculus r o t o n d u s and also t h e last 3 cm of the distal ileum, a p h e n o m e n o n already o b s e r v e d b y Alvarez [ 1 ] . A s c e n d i n g cecal c o n t r a c t i o n s spread t o w a r d s the ileum a n d are c o n c o m i t a n t w i t h i n h i b i t i o n of ileal spiking activity (Fig. 4, u p p e r panel). S o m e d i r e c t p r o p a g a t i o n s of c o n t r a c t i o n s f r o m the i l e u m to t h e c o l o n involving only the a m p u l l a cecalis were also recorded. This p a t t e r n as well as the i n h i b i t o r y e f f e c t o n t h e ileum b y an a s c e n d i n g cecal c o n t r a c t i o n was very n o t i c a b l e (Fig. 4, l o w e r p a n e l ) d u r i n g the passage o f a m i g r a t i n g m y o e l e c t r i c c o m p l e x (regular spiking a c t i v i t y ) o n t h e t e r m i n a l ileum [ 13].

Electrical Activity o f the Fusus C,/i and Ad/oining Colon Mean values o f the slow-wave f r e q u e n c y s h o w e d a n increased g r a d i e n t f r o m oral t o a b o r a t p a r t s o f t h e p r o x i m a l colon. A c o n t i n u o u s h i g h f r e q u e n c y was m a i n t a i n e d atong the whole distal c o l o n in r a b b i t s regardless o f feeding p a t t e r n s (Table 3). S e c t i o n of t h e gut i m m e d i a t e l y oral to the fusus coli [23] resulted in the f r e q u e n c y o f t h e slow waves o f the p r o x i m a l c o l o n being halved b u t t h e g r a d i e n t was m a i n t a i n e d . Spiking activity o c c u r r e d e i t h e r as series of bursts or single b u r s t s p r o p a g a t e d o n t h e distal c o l o n at a velocity of 0.4 c m / s e c d u r i n g t h e interdigestive p e r i o d (Table 3 t.

Changes in the Electrical Activity n f the Large Intestine with Feeding and Ceeotroph.v During feeding t h e p r o x i m a l c o l o n , the fusus coli and to

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FIG. 3. Ceco-colic electrical activity (and diagrammatic representation of same) incorporaUng the major patterns of propagated spike bursts on the cecum and the colon (black arrows) and those restricted to either cecum or colon ~white arrows) in a rabbit ted ad lib. Electrode sites as in Fig. 2~

COLON MOTILITY AND CECOTROPHY

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H G . 4. Patterns of electrical activity at tile ileo-cecal junction. Electrode sites include thc telminal ileum 10 cm [11 and 2 cm [2] anterior to the sacculus rotondus, tlre sacculus rotondus [31, the ampulla cecalis 5 cm apart [4,5] and the ceco-colic junction [61. Inset shows three major con lraction pathways. Contractions labelled A (white), shown at a high recording speed on the upper panel arc descending cecal contractions diverging to spread over the ampulla cecalis [4,5] and through the saccutus rotondus [3] to activate the distal ileum [2]. Conlractions labelled B (black) are ascending cecal contractions traversing the ampulla cecalis [4,5] and diverging to spread through the sacculus rotondus to inhibit the distal ileum [1,21 ; this contraction is shown at both high (upper panel) and low (lower panel) recording speeds. Contractions labeled C (dots) correspond to ileal contractions propagated directly through the sacculus rotondus [3] to tire ampulla cecalis [4,5] and then the cohm [61.

TABLE

3

SLOW-WAVE FREQUENCY ALONG THE COLON AND MEAN VELOCITY OF PROPAGATION OF SPIKE BURSTS FROM 8 SITES LOCATED AT 1 CM TO 70 CM FROM THE ILEO-CECOCOLIC JUNCTION IN 3 RABBITS OF GROUP B (MEAN VALUES FOR NONFEEDING PERIODS DURING 24 HR, 10 DAYS AFTER ELECTRODE IMPLANTATION) Junction cm

Oral 15

1

Proximal colon Aboral 20

Slow-wave frequency (per rain) Mean 13.8 16.3 ± S.D. ± 0.7 _+ 0.4 Velocity (cm/sec) Mean _+ S.D.

1.41 _+ 0.27

17.0 ± 0.4 1.37 _+ 0.17

Fusus coil

Distal colon

25

37

39

50

70

17.4 ± 0.7

18.1 ± 0.4

19.3 _+ 0.6

22.6 _+ 0.4

19.4 + 0.9

1.42 -+ 0.18

0.41 -+ 0.12

0.61 _+ 0.19

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FIG. 5. Electrical activity of the cecum and colon in a rabbit fasted tbr 18 hr. during feeding and cecotrophy. are measured from the ceco-colic junction. Note the overall increase in spiking activity, incorporating both with feeding. The tracings during cecotrophy show an inhibition of the proximal colon and corresponding distal colon. The spread of individual propagated contractions is increased from 0.4 in the fasted rabbit to 0.8 a lesser e x t e n t t h e distal c o l o n d e v e l o p e d an increased spiking activity (Fig. 5). During the first 2 hr of the p o s t p r a n d i a l period, the level o f spiking a c t i v i t y o n the p r o x i m a l c o l o n was a b o u t twice t h a t seen o n the distal colon. This p a t t e r n c o r r e s p o n d e d to a transit time for the c o l o n o f 150 rain [ 12] o n t h e distal colon. The velocity of p r o p a g a t i o n of some spike b u r s t s was increased by 25%. No significant changes in slow-wave f r e q u e n c y were recorded.

I *tJt4i'lt'~lt

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Distances of electrodc site~ proximal and distal colon. increase m activity on the cm/sec during cecotrophy.

At the b e g i n n i n g o f c e c o t r o p h y , tile activity o f the colon was a b r u p t l y m o d i f i e d . A relatively low level o f spiking activity o n b o t h the cecal base and the oral p a r t o f p r o x i m a l c o l o n was r e c o r d e d , w h e r e a s the distal c o l o n e x h i b i t e d a h i g h level o f activity. The velocity of propagation of the spike b u r s t s was increased by 5 0 ~ w i t h o u t m a j o r c h a n g e s in slow-wave f r e q u e n c y ( F i g 5 ) Q u a n t i t a t i v e e v a l u a t i o n o f the spiking activity s h o w e d

C O L O N M O T I L I T Y AND C E C O T R O P H Y

877

ILEUM ~ O X I M A L COLON F.COLI CECUM i ',*', l . ' ~ ~ ~ EIect rode ~ c ' m " " 2 0 mc ~ 6 cm Length cm ..--15 - - - - , 4 - - 2 0 .-~5~ =

DISTAL COLON 115cm

49cm -

-

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I00

COLON

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soft pellets 1"4

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1"8

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soft pellets 2"2

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FIG. 6. Frequency of contractions of the cecal base and spiking activity of the colon are shown as percentages per 2 rain periods. Distances of electrode sites and the length of the different parts of the colon are measured from the ceco-colic junction. Cecal activity is increased before and during feeding with a period of increased activity of the proximal colon and ji~s'us colt ihatched area). A band of increased activity (dotted area) moves slowly from the aboral part of the proximal colon along the distal colon and emission of" soft pellets occurs when it reaches tl~e rectum. A second similar pattern is seen 4 hr later. that successive high levels of activity on the p r o x i m a l and distal colon t o o k the form of bands o f activity which reached the r e c t u m within 3 hr and were followed by the emission o f soft pellets. When a s e c o n d elimination o f soft pellets o c c u r r e d , the band activity started at the level o f the aboral part o f the p r o x i m a l colon where it seemed to migrate slowly over the .[i~sus colt and distal colon (Fig. 6). DISCUSSION

E l e c t r o m y o g r a p h i c studies o f c o l o n m o t i l i t y have s h o w e d that antiperistalsis, which is restricted to the oral part of the p r o x i m a l colon, is u n m o d i f i e d during the period of soft pellet p r o d u c t i o n , i.e. f r o m 2 to 4 hr prior to their elimination [181. On the o t h e r hand, during this period,

the jhsus colt e x h i b i t s no spiking activity differing markedly from that o f the nearby colon, indicating that it does not play a significant role in the variation of fecal water content. The slow waves which exist on the entire colon 16,16] exhibit, as in the cat [ 5 ] , a reverse gradient of their f r e q u e n c y on the p r o x i m a l colon, with the fusus colt as the p a c e m a k e r [ 2 3 ] . This offers an e x p l a n a t i o n for the mechanical separation of liquid and solid digesta resulting in a c o n c e n t r a t i o n o f coarse particulate m a t t e r m o r e than twelve t i m e s as high in the colon as in the cecum [31; c o n t i n u o u s weak c o n t r a c t i o n s at the same f r e q u e n c y as the slow waves may squeeze out tile fluid and the fine dry m a t t e r front colonic c o n t e n t s and t r a n s p o r t them from h a u s t r u m to h a u s t r u m , from the ./usus c(,li t o w a r d s the

878

R U C K E B U S t ? H AND H{:)RNICKE

initial part o f the p r o x i m a l c o l o n and t h e n to the c e c u m by antiperistalsis. H o w e v e r since n o changes in the slow-wave f r e q u e n c y are r e c o r d e d during soft pellet p r o d u c t i o n such a m e c h a n i s m is n o t likely to be involved in the p r o d u c t i o n of soft pellets. In c o n t r a s t , a time relationship exists b e t w e e n the p r o d u c t i o n o f hard and soft pellets c o n c o m i t a n t with an initial increase t h e n a decrease in spike activity o f the p r o x i m a l colon. The decrease w h i c h occurs s u d d e n l y on the aboral part o f the p r o x i m a l colon and the f u s u s coli during the emission of soft pellets is c o n c o m i t a n t with an increase in the activity o f the distal colon. This p r o b a b l y indicates that soft pellet p r o d u c t i o n c o r r e s p o n d s to an e m p t y i n g o f the p r o x i m a l colon and possibly of the cecum. F o r a fast propulsion o f t h e c o n t e n t s from the p r o x i m a l to the distal colon, a p r e r e q u i s i t e seems to be that the mass of hard

pellets stored in the distal c o l o n be eliminated. l'hc ~v,eratl increased activity regularly observed on the small intestine [241 and cecum [~vt--- during feeding and ,the e a r b p o s t p r a n d i a l period, may facilitate a s u b s e q u e n t filling of the colon. Ii is suggested t h a t the proximaI colotl is the key site m solving the enigma of the p r o d u c t i o n o f the two kinds oi feces. A c o u n t e r c u r r e n t w i t h the lu.vua c,)~i as the p a c e m a k e r area is responsible for the mechanical s e p a r a t i o n o f liquid and solid digesta. The p o s l p r a n d i a l elimination o i hard feces a c c u m u l a t e d in the dislal colon possibly triggers an increased activity orad to the [}lsus coil and its migration to the distal colon, t h u s p e r m i t t i n g the rapid passage o f the c o n t e n t s , ie. soft pellets from the prox~mat to distal c o l o n and rectu m

REFERENCES 1. Alvarez, W. C. Further studies on intestinal rhythnL Am. J. Physiol. 37: 2 6 7 - 2 8 l , 1915. 2. Auer, J. Further note on the fllsus coil of the rabbit. Proc. Soc. exp. Biol. Med. 22:301 303, 1925. 3. Bj6rnhag, G. Separation and delay of contents in the rabbit colon. Swedish J. agr. Res. 2 : 1 2 5 - 136, 1972. 4. Bonnafous, R. and P. Raynaud. Recherches sur le r61e du c61on dans la dualitd de l'excr6tion f~cale du lapin. Archs Sci. Physiol. 21:261 270, 1967. 5. Christensen, J., Anuras and R. Hauser. Migrating spike bursts and electrical slow waves in the cat colon: effect of sectioning. Gastroenterology 66: 240-247, 1974. 6. Couturier, D., C. Roze, M. It. Couturicr-Turpin, et al. Electromyography of the colon in situ: an experimental study in man and in tim rabbit. Gastroenterology 56: 317-322, 1969. 7. Eden, A. Coprophagy in the rabbit: origin of "night" feces. Nature 145: 628, 1940. 8. Elliott, T. R. and E. Barclay-Smith. Antiperistalsis and other muscular activities of the colon. J. Physiol., Lond. 31: 272-304, 1904. 9. Ferrando, R., R. Wolter, J. C. Vilat and J. P. Megard. Teneur en acides amines des deux categories de f~}ces du lapin: caccotrophes et f~ces dures. C.r. hebd. Sg'anc. Aead. Sci., Paris 270: 2202-2205, 1970. 10. l:ioramonti, J. and Y. Ruckebusch. La rnotricitd caecale chcz Ic lapin. I. Nature des contractions. Annls Rech. v~t. 5 : 1 13, 1974. 11. Fioramonti, J. and Y. Ruckebusch. La motricit~ caecale ehez te lapin. It, Variations d'origine alimentaire. Annls Rech. v&. 5: 201-212, 1974, 12. Fioramonti, J. and Y. Ruckebusch. La motricit~ caecale chez le lapin. III. Dualit6 de l'exer~tion fgcale. Annls Rech. v&. 7: 216-228, 1976. 13. Grivel, M. L. and Y. Ruckebusch. The propagation of segmental contractions along the small intestine. J. Physiol.. Lond. 227:611 - 625, 1972. 14. Harder, W. Zur Morphologie mad Physiologie des Btinddarms der Nagetiere. Verh. Deutseh. Zool. EA'p. 2: 95- 109, 1949.

15

16.

17. 18. 19. 20. 21. 22.

23. 24.

25.

26.

27. 28.

[-16rnicke. I1. and G. Folkmitt. St¢fffwechselk~fig mit elektronischer Steuerung zm fraktionieNen Sammlung yon Kot und Coecotrophe beim Kaninchen. Z Tierphy.~[ol. 31: 107 110. 1973. Jute. Y. Etude in vitro de l'activilc electromyographique du c61on proximal el distal du lapin .L Ph~siol. Paris 68: 305 329. 1974. I,ebas. [:. and J. P. Laplace. Sur l'excrction f~cale chez le lapin. lnnls Zootech. 23: 5 7 7 - 5 8 t . 1974. Leng, t'. and H. H6rnicke. Tagesrhyrmische Unterschiede m der Zusammensetzung des Blinddarminhalts yon Kaninchen. Z. I/ersuchstierkde 17: 285--299. 1975. Morot. C. Pelotes stomacales des ldporides. Rec. Med. v&. 59: 635 645. 1882. Myers. K Coprophagy of flw European rabbit m Australia. Aust. J. Zool. 3: 336--345. 1955. Pickard D. W. and C. E. Stevens. Digcsta flow through the rabbit large intestine. Am. J. Physiol. 222:1161 1166. 1972 Ruckebuscb. Y. and M. L, Grivel. Etude de la motriciK caecale chez le [apir dveilld: variations spomandes er provotm~;es Th~rapie 22:1477 -1486. 1967. Ruckebusch. Y. and J Fioramonli. Ttw fusus coil of the rabbit as a pacemaker area. Experientia 32:1023 1024, I976. Ruckebusch. Y.. Grivel. M L. and M. J I,'argeas. Activild dlectrique de l'intestin et prise de nourriture conditionnetlc cbez le lapin. Physiol. Behav. 6:359 366. 1971. Ruhlaud. M and H. J. I;hrlein. Bewegungsvorgange am Blinddarm des Kaninchens und ibre circadiane Rhythmik. Z. l'ierphys#)l. 3 0 : [ 2 2 - 1 2 3 1972. Taylor. ~. I.. The demonstration oi a peculiar kind ,at coprophagy normally practised by rne rabbit. Vet. Rec. 52: 259-~ 262. 1940. I'hacker. E..! and C. S. Brandt. Coprophagy m lie rabbi1. J. Nutr. 55: 375 3 8 5 . 1955. Watson. J. S. and R. H. Taylor. Reinfection in the hare. Lepus europeanus. Science 121: ~14. 1955