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THE DIGESTIVE SYSTEM OF
VERTEBRATES: CD 
6. Motor activity of the digestive tract:
Introduction:
The reduction of food to a small particle size, mixing of ingesta with digestive fluids and enzymes, and movement of digesta through the digestive tract are performed principally by its motor or muscular activity. Frogs, anteaters, and cattle use their tongue for the prehension or capture of food. Many vertebrates use their teeth, horses use their lips, and most primates use their hands for this this purpose. Food can be reduced to a small particle size by microfiltration, the cutting, tearing, crushing, or grinding activity of teeth and jaws, or by the muscular activities of the foregut. Ingesta is passed through the esophagus of some fish, amphibians and reptiles with the aid of cilia. However, with the exception of embryonic fish and larval amphibians, ingesta is transferred through the digestive tract principally or entirely by muscular activity. The initial stages of ingestion and final stage of fecal elimination are accomplished by striated muscle under voluntary control. The motor activities in the remainder of the digestive tract are conducted by smooth muscle, which contracts more slowly, shows a greater range of distention or tonus, and is under the involuntary control of the muscle cells, hormones, paracrine agents, and the intrinsic nervous system of the digestive tract.
Headgut:
Movements of the jaws and tongue, and the initial stage of deglutition (swallowing) are voluntary and activated by striated muscles, but the pressure of food against the pallet and pharynx stimulates a nervous reflex that involves a deglutition (swallowing) center in the brain stem. This results in a complex series of events that pass food into the esophagus (Davenport 1982; Goyal and Paterson 1989).
Foregut - Esophagus:
The esophagus and gastrointestinal tract of most vertebrates are invested with an inner layer of circular muscle and outer layer of longitudinal muscle. The circular muscle forms a well defined sphincter at the gastroesophageal junction of some fish, adult amphibians, reptiles, and mammals, but this region is delineated only by a muscular constriction in many species (Botha 1958, 1962). The longitudinal layer of muscle is incomplete near the gastroesophageal junction of some adult amphibians and reptiles. These muscles are striated in the esophagus of fish and over varying lengths of the mammalian esophagus. However, the esophagus of amphibians, reptiles, and birds, and terminal esophagus of most mammals is invested with smooth muscle.
Boluses of food are passed through the esophagus and into the stomach by peristaltic waves of esophageal muscle contraction. Antiperistaltic waves of contractions are also seen in the esophagus of some birds and mammals. They aid in the regurgitation of crop contents for the feeding of young in some species of birds, the regurgitation of undigested waste products from the gizzard of raptors such as hawks and owls, and the regurgitation of forestomach digesta in ruminants and camelids. Antiperistaltic contractions also accompany the eructation (belching) of gas produced in the forestomach of ruminants and camelids (Sellers and Stevens 1960) and stomach of dogs (Heywood and Wood 1988).
The pressure events associated with deglutition, eructation, and the regurgitation phase of rumination in the bovine esophagus are shown in Figure 6.1. Deglutition is associated with a wave of peristaltic contraction, which terminates with relaxation of the gastroesophageal sphincter and transfers the food bolus through the esophagus and into the forestomach. However, regurgitation and eructation are accompanied by antiperistaltic waves of esophageal contraction. Regurgitation is preceded by a drop in intrathoracic intraesophageal pressure, due to inspiration against a closed glottis, and accompanied by relaxation of the gastroesophageal sphincter and aspiration of digesta into the thoracic esophagus. Eructation is also preceded by relaxation of the sphincter, but rumen gasses are forced into the esophagus by contractions of the abdominal muscles (abdominal press) and rumen.
Figure 6.1 Esophageal pressure events during bovine (A) deglutition, (B) regurgitation, and (C) eructation.. Numbers represent 1) cervical esophagus 79 cm cranial to cardia, 2) thoracic esophagus 40 cm cranial to cardia, 3) thoracic esophagus 19 cm cranial to cardia, and 4) pleural cavity. The peristaltic deglutition wave is accompanied by no changes in respiratory cycle. However, regurgitation is accompanied by a marked drop in pressure in the pleural cavity and thoracic esophagus, followed by an antiperistaltic wave of esophageal contraction. Eructation is recorded as a rise in intrathoracic pressure of low amplitude and approximately one-second duration, due to abdominal press. This is followed by a high pressure, short duration wave of antiperistaltic esophageal contraction, often followed by a fluid- clearing wave of deglutition. (From Sellers & Stevens 1960)
Most mammals can remove irritating or toxic substances from their stomach by emesis or vomiting. Chemical or physical irritation of the gastrointestinal tract can initiate a nervous reflex via an emetic center in the medulla. This results in relaxation of the esophageal sphincters, contraction of the longitudinal muscles of the esophagus, an increase in the tonus of stomach muscles, contraction of abdominal muscles (abdominal press), and the ejection of gastric contents. However, there is no evidence of esophageal antiperistalsis that accompanies rumination and eructation during emesis in humans or other species (Botha 1958, 1962). Rats, horses, and ruminants are unable to vomit. Rats appear to have compensated for this by a highly developed sense of taste and smell, and ruminants eject abomasal contents into the forestomach during abomasal displacement or torsion. However, horses will often rupture their stomach before vomiting.
Foregut - Stomach:
The stomach of most vertebrates is invested with an outer layer of longitudinal muscle and an inner layer of circular muscle, which forms a pyloric valve or sphincter at its junction with the midgut. A third, oblique layer of muscle is found near the esophageal junction of some mammals, and the longitudinal muscle is almost absent in the gizzard of birds and concentrated in longitudinal bands over most of the stomach of macropod marsupials and colobid monkeys (Fig. 5.19b and c). The muscular arrangement of the ruminant forestomach is very complex.
Figure 5.19b Eastern grey kangaroo (Macropus giganteus) digestive tract (Stevens & Hume 1995)
Figure 5.19c Colobus monkey (Colobus abyssinicus) digestive tract (Stevens & Hume 1995)
In most vertebrates, the circular muscle in the cranial portion of the stomach undergoes receptive relaxation at the time of a meal. This is followed by periodic, stationary contractions of the circular muscle, which mix and macerate gastric contents. However, the motor activity of distal stomach is dependent on slow, rhythmic cycles of partial depolarization of the membrane potential of its muscle cells (Fig. 6.2). This basic electrical rhythm (BER) is initiated by pacemaker cells that are located near the axial center of the stomach and generate slow waves of depolarization in the membranes of the circular muscle cells in the distal stomach. Although the BMR does not in itself initiate muscular contraction, it sensitizes these cells to contract under extrinsic, neurohumoral stimulation. When stimulated, these slow waves are accompanied by spike potentials of more complete membrane depolarization, which result in peristaltic waves of muscular contraction that mix digesta in the distal segment of the stomach and eventually transfer gastric contents into the midgut during periods of pyloric sphincter relaxation. These two type of motor activity appear to apply to the stomach of all simple-stomached vertebrates.
Figure 6.2 Basal electrical rhythm of the human stomach. Slow waves of partial depolarization of the circular muscle is initiated by a pacemaker and passes over the distal half of the stomach. These initiate contractions when accompanied by spike potentials. (Stevens 2001)
The forestomach contractions of macropod marsupials also appears to be influenced by a basic electrical rhythm. Fluoroscopic studies of the tammar wallaby showed that contractions of the haustra of the macropod marsupial forestomach (see Fig. 5.19b) spread in an aboral direction with an intermittent narrowing of the haustra (Richardson and Creed 1981). A basic electrical rhythm of 5-6 cycles per minute was recorded along the entire stomach of the tammar wallaby and quokka, and this was accompanied by aborally-moving waves of haustral contraction of the same frequency (Richardson and Wyburn 1983, 1988). The motor activities of the hoatzin, sloth, colobid monkeys, and hippo forestomachs do not appear to have been examined. However, studies of the ruminant and camelid forestomach have demonstrated a unique combination of complex, involuntary motor events that are under central nervous system control.
Figure 5.19b Eastern grey kangaroo (Macropus giganteus) digestive tract (Stevens & Hume 1995)
The motor activities of the ruminant and camelid forestomach are complex and closely integrated with rumination (regurgitation, remastication, and reswallowing of digesta) and the eructation (belching) of gas. The stomach of advanced ruminants, is divided into a multicompartmental forestomach (reticulum, rumen and omasum), and a secretory compartment (abomasum) similar to the entire stomach of most other species (Fig. 6.3) The foretomach consists of a large reticulorumen, which serves as the major fermentation organ, and an omasum, which transfers digesta from the reticulum into the abomasum. Closure of a ventricular groove that runs from the gastroesophageal juncture (cardia) to the abomasum, allows milk to bypass the forestomach of nursing calves, but this becomes inoperative following weaning. The ventral location of the reticulo-omasal orifice and a filter formed by thin, projecting leaves of omasal tissue prevents the passage of large digesta particles in older animals.
Figure 6.3 Diagrammatic sections of bovine reticulorumen and omasum. Structures and compartments of major importance are numbered as follows: 1) cardia, 2) reticulo-omasal orifice, 3) reticulum, 4) cranial sac of rumen, 5) dorsal sac of rumen, 6) caudodorsal blind sac, 7) ventral sac of rumen, 8) caudoventral blind sac, 9) ruminoreticular fold, 10) cranial pillar, 11) right longitudinal pillar, 12) caudal pillar, 13) dorsal coronary pillar, 14) ventral coronary pillar, 15 ) omasum, 16) omasal canal, 17) omasal pillar, 18) omaso-abomasal orifice, 19) omasal lamina (leaf), 20) abomasum. (From Sellers & Stevens 1966.)
The pressure events associated with muscular contractions of the bovine forestomach, in the absence of feeding or rumination, are illustrated in Figure 6.4. The reticulum, rumen, reticulo-omasal sphincter, and omasal canal undergo a continuous series of cyclic contractions (Sellers and Stevens 1960). Each cycle is initiated with a double contraction of the reticulum and followed by a primary wave of contraction that spreads over the dorsal and ventral sacs of the rumen, the reticulo-omasal sphincter, and the omasal canal. These cycles may include a secondary wave of contraction, which includes all of these structures other than the reticulum. The body of the omasum also undergoes powerful contractions, but these are neither cyclic in nature nor necessarily present during each cycle.
Figure 6.4 A six-minute recording of reticuloruminal cycles and associated events in the esophagus and omasum. Note the relationship between the contractions of the rumen and omasal canal, and the prolonged, acyclic contractions of the omasal body pressure during primary contraction of the dorsal rumen and omasal canal. Upper traces show eructation as a biphasic wave occurring during secondary rumen contractions and the frequent waves of deglutition associated with the swallowing of saliva. (From Sellers & Stevens 1966.)
The cyclic contractions of the reticulum and rumen serve to mix and circulate digesta in the reticulorumen (Fig. 6.5). Cyclic contractions of reticulo-omasal sphincter and omasal canal aid in the passage of digesta from the reticulum into the omasal canal and body, as shown in Figure 6.6. The second reticular contraction draws the reticulo-omasal orifice and omasal canal downward, first closing the orifice and reducing the pressure within the canal and then opening the orifice at the time of maximum reticular contraction. This results in a small, but rapid aspiration of digesta from the floor of the reticulum. The primary and secondary contractions of the reticulo-omasal sphincter and omasal canal force fluid and small particles of digesta from the canal into the spaces between the leaves of the omasal body, leaving the larger particles in the canal. The subsequent relaxation of these structures results in a negative pressure, which aspirates more copious amounts of digesta from the reticulum into the omasal canal. When these cycles of aspiration and contraction have distended the omasum to a sufficient degree, it undergoes a strong, prolonged contraction. These contractions pass most of its contents into the abomasum and small amounts of digesta back into the reticulum, along with the larger particles retained by the filter of omasal leaves. Thus, the omasum serves as both a pump for the transfer of digesta from the reticulum into the abomasum and a filter to retain the larger particles for further fermentation in the reticulorumen.
Figure 6.5 Movement of digesta during primary and secondary contractions of the reticuloruminal cycles. (From Stevens & Hume 1995.)
Figure 6.6 Movement of digesta through the bovine omasum. Closed arrows show movement of digesta and open arrows show movement of forestomach walls. Diagrammatic axial section (see Fig. 5.3) shows the cranial reticulum (1), reticulo-omasal orifice (2), omasal leaf portion of omasal body (3), omasal canal (4) and cranial abomasum (5). A: All structures are relaxed during much of the cyclic contraction of the forestomach. B: During the second reticular contraction, the reticulo-omasal orifice and omasal canal are pulled ventrally, producing a negative pressure in the canal and a closing and then opening of the orifice, which results in aspiration of digesta from the base of the reticulum. C: Primary contraction of the rumen is associated with a primary contraction of the reticulo-omasal orifice and omasal canal, forcing fluid and small digesta particles between the leaves of the omasal body and into the abomasum. These events are followed by relaxation of these structures (D), and repeated if the forestomach undergoes a secondary contraction. E: At intervals that vary and are unrelated to the cyclic contractions of the forestomach, a wave of contraction passes over the omasal body, releasing its contents into the abomasum. (From Stevens & Hume 1995.)
The reticulorumen contains a layer of larger plant particles floating on a more fluid layer of smaller, partially digested particles and capped by a pocket of the gasses produced by microbial fermentation. Eructation of gas occurs during contraction (generally the secondary) of the dorsal sac of the rumen, when the cardia region (antrum) is exposed to the gas pocket as a result of the reticular contractions and contraction of the cranial pillar.
Ruminants and camelids are unique in their ability to ruminate, which consists of the regurgitation, remastication, and reswallowing of digesta in the floating layer of their forestomach at intervals throughout the day. Rumination is stimulated by the presence of course particles of plant fiber pressing against the antrum of the rumen and inhibited by physical or psychological stress. It aids in the further mastication and maceration of plant material, under less stressful or dangerous conditions, and it has been estimated that rumination in a recumbent position can conserve up to 10% required for forage intake by sheep (Gordon 1968).
Both rumination and eructation are tightly integrated with the cyclic contractions of the forestomach. During rumination, the bolus is regurgitated only at the time of an extra reticular contraction, which begins these rumination cycles, and the remasticated bolus is never swallowed until completion of the cycle (Fig. 6.7). Eructation occurs only during contraction of the dorsal sac (Fig. 6.4), even if the rumen is completely emptied of digesta and infused with gas at a pressure of 20 mm Hg (Stevens 1958). This integration of rumination and eructation with the cyclic contractions of the forestomach is controlled by nerve centers in the medullary region of brain, and all three of these activities cease following severance of the vagal nerve trunks. Therefore, other than emesis, it represents the only known example of direct central nervous system control of gastrointestinal functions and it is one of the most complex series of involuntary motor events witnessed in animals.
Figure 6.7 Reticuloruminal cycles during rumination in cattle. Numbers 1 and 2 mark first and second reticular contractions seen with every cycle and the x marks the extra reticular cycle at the regurgitation stage (R) of rumination. The remasticated bolus is swallowed (D) just prior to the next reticulorumen cycle. The AP on the reticular tracing is a registration of abdominal press at the time of eructation (E). (From Stevens & Sellers 1968.)
Figure 6.4 A six-minute recording of reticuloruminal cycles and associated events in the esophagus and omasum. Note the relationship between the contractions of the rumen and omasal canal, and the prolonged, acyclic contractions of the omasal body pressure during primary contraction of the dorsal rumen and omasal canal. Upper traces show eructation as a biphasic wave occurring during secondary rumen contractions and the frequent waves of deglutition associated with the swallowing of saliva. (From Sellers & Stevens 1966.)
The forestomach of camelids undergoes a somewhat similar series of contractions, which are also integrated with eructation and rumination. The camelid stomach is divided into three compartments. The first two compartments are analogous to the reticulorumen, and the third compartment is analogous to the abomasum (Fig. 6.8). A ventricular groove provides a similar shunt for the passage of milk in nursing animals. The first compartment is bisected partially by a muscular pillar, and both it and the second compartment are lined with stratified squamous epithelium plus regions of glandular pouches (Fig. 6.9).
Figure 6.8 Schematic representation of the llama stomach. The esophagus (1) enters the first compartment (A), which is partially divided into cranial (3) and caudal (4) sacs by a pillar of muscle (7), and separated from the second compartment (B) by a constriction (8). Both compartments include regions of saccules (5,6,9) containing cardiac glandular mucosa. A ventricular groove (2) runs along the lesser curvature of the forestomach between the esophagus and the third compartment (C). The initial four-fifths of the third compartment is also lined with cardiac glandular mucosa (11,12). The terminal segment (13) is lined with proper gastric mucosa and separated from a duodenal ampulla (D), by a pyloric sphincter (14). (From Vallenas et al. 1971.)
Figure 6.9 Left, lateral, longitudinal section of the llama stomach showing the entrance of the esophagus (A), transverse pillar (B) between the cranial and caudal sacs of the first compartment and entrance to the second compartment (C). It also shows the openings to the glandular saccules in the first compartment. (Modified from Vallenas et al. 1971.)
The first and second compartment undergo cyclic waves of contraction. However, they start with a single contraction of the second compartment and progress with multiple contractions of the caudal and then cranial sac of the first compartment (Fig. 6.10). The regurgitation phase of rumination was associated with an extra contraction of the cranial sac and eructation was associated with contractions of the caudal sac of the first compartment. Each contraction was accompanied by eversion of the glandular pouches (Fig. 6.11). Therefore, the camelid and ruminant forestomachs demonstrate a number of analogies, and the glandular pouches of the camelid forestomach are remindful of the glandless pouches of the ruminant reticulum. However, the camelid forestomach lacks an omasum, and other differences discourage use of the terms reticulum and rumen.
A process called merycism, with some of the characteristics of rumination, has been described in macropod marsupials, dasyurids, and most recently the koalas (Logan 2001). However, it appears to consist of either regurgitation without mastication or mastication without regurgitation.
Figure 6.10 Pressure recording of cyclic contractions of llama forestomach. (From Vallenas & Stevens 1971a.)
Figure 6.11 Cyclic contraction of the first compartment of the llama forestomach. A-D show contractions of pillar and sacs. Cyclic eversion of caudal sac pouches during the three stages of contraction is shown in drawings on the right. (From Vallenas & Stevens 1971a.)
Midgut:
The midgut is invested with an outer longitudinal and an inner circular layer of muscle (Fig, 4.6). The circular muscle forms a valve or sphincter at its juncture with the hindgut of a few fish, some adult amphibians, and the reptiles, birds, and most mammals. Digesta are mixed and moved through the midgut by a gradation in the frequency of standing waves and of muscular contraction and peristaltic rushes. The midgut of mammals can be subdivided into progress segments of duodenum, jejunum and ileum. The BER of the intestinal circular muscle cells of cats decreased in a stepwise fashion, from 18/minute in the duodenum to 12.5/minute in the terminal ileum (Davenport 1982). However, no gradation was seen in the midgut of guinea pigs (Calligan et al. 1985). Neuro or humeral stimulation of these muscle cells result in their contraction, which mixes digesta and passes it short distances down the tract.
Figure 4.6. Cross-section of the intestine. (Stevens 2001.)
Passage of digesta along the midgut is also aided by migrating myoelectric complexes (MMC) that generate peristaltic rushes. The three phases of migrating myoelectric complexes in the dog and human are illustrated in Figure 6.12a, b, c. Phase I is a quiescent period when the slow waves are unaccompanied by contraction, but they are accompanied by action potentials and muscular contractions intermittently in phase II and continuously in phase III (Fig. 6.12a). Feeding resulted in a shortening of Phase I and prolongation of phase II in the midgut of dogs and humans (Figs. 6.12b, c). However the MCC pattern was uninterrupted in the herbivorous horses, ruminants, and macropod marsupials (Ruckebusch 1981; Richardson and Wyburn 1983), which tend to feed almost continuously. The MCCs of the omnivorous pig were similar to those of the dog and human on concentrate diets fed three times a day and similar to that of herbivores when fed a high fiber diet.
Figure 6.12a Phases of migrating myoelectric complexes (MMC) during interdigestive (fasting) and feeding periods in carnivores and humans. This diagram shows slow waves with no spike potentials during phase I, intermittent spike potentials during phase II, and consistent spike potentials during phase III. (From Hendrix 1987.)
Figure 6.12b Phases of migrating myoelectric complexes (MMC) during interdigestive (fasting) and feeding periods in carnivores and humans. This diagram shows the effects of interdigestive periods on the MCC, which originate in the stomach and lower esophageal sphincter (LES) and pass through the small intestine. (From Hendrix 1987.)
Figure 6.12c Phases of migrating myoelectric complexes (MMC) during interdigestive (fasting) and feeding periods in carnivores and humans. This diagram shows the effects of feeding on the MCC, which originate in the stomach and lower esophageal sphincter (LES) and pass through the small intestine. Feeding interrupts the cycle and increases the duration of phase II. (From Hendrix 1987.)
The velocity and number of MMC per day varies with species. Both appear to increase with the length of the intestine (Fig. 6.13). However, while they were limited to the interdigestive periods in carnivores and humans, they were distributed throughout the day in herbivores. Oral transmission of MCCs was also recorded in the midgut of chickens (Roche and Ruckebusch 1978), and antiperistaltic waves of contraction are a relatively common feature of the avian midgut (Duke 1986). They also have been observed in the midgut of some mammals
Figure 6.13 Relationship between the velocity of propagation of myoelectric complexes and the length of the small intestine. The hatched area shows the 95% confidence limits. The median daily number of jejunal complexes is high in ruminants and low in carnivores, because of the obliterating effect of feeding in the latter species. (From Ruckebusch 1981.)
Hindgut:
The hindgut also mixes digesta with muscular contractions and moves digesta both aborally by peristalsis and orally by antiperistalsis. Antiperistaltic waves of contraction that are generated in the cloacal region and pass over the length of the hindgut have been observed in the tortoise Geoclemys reevisii (Hukuhara et al. 1975), and chickens, turkeys, Japanese quail, and roadrunners (Stevens and Hume 1995). Myoelectric studies also indicated a progressive increase in the frequency of slow waves from the ileocecal junction to the cloaca in the opossum (Anuras and Christensen 1975). However, the digestive tracts of most mammals develop separate exits prior to birth and the colon is generally longer, with its pacemaker located in a more proximal segment.
Early studies showed antiperistalsis in the proximal colon of the cat, ferret, rat, guinea pig, and rabbit (Elliott and Barclay-Smith 1904), and a simultaneous contraction of distal cat colon that resulted in a mass movement of its contents into the rectum (Cannon 1902). A basal electrical rhythm similar to that of the midgut was recorded in the hindgut of cats, but their frequency increased from the ileal-cecal-colonic junction to the midcolon and remained constant over the remaining length of distal colon (Fig. 6.14). Sellers et al. (1982) reported a pair of pacemakers at the junctions of both the ventral and dorsal colon, and the dorsal and small colon of the pony.
Figure 6.14 Relationship between digesta flow and electrical slow waves and migrating spike bursts in the cat colon. Slow waves (SW) appear to originate from a pacemaker midway along the colon, spread toward the cecum, and tend to produce digesta flow in the same direction. Migrating spike bursts (MSB) begin at a variable position in the proximal colon and migrate toward the rectum. These are accompanied by contractions, which tend to move digesta in that direction. (From Christensen et al. 1974)
Therefore, the hindgut undergoes mixing contractions, and contractions of the distal colon that move digesta into the rectum. It also undergoes periodic waves of antiperistaltic contraction which can reflux digesta and cloacal urine the length of the hindgut in some reptiles and birds (Fig. 4.6) or reflux digesta the length of the proximal hindgut in most mammals (Fig. 5-10).
Figure 4.6. Cross-section of the intestine. (Stevens 2001.)
Figure 5.10. The large intestine of the human, dog, horse, pig and Ox. Note that the cecum and segments homologous to the ascending, transverse and descending colon of humans vary in their relative length, shape, and volume, and that the proximal or "ascending" segment is extended and expanded in many mammals. (Modified from de Lahunta and Habel 1986.)
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