Myoelectric Activity at the Gastroduodenal Junction #

The presence of rhythmic electrical activity in the musculature of the gastric "antrum" of anaesthetized dogs was first reported by Alvarez and Mahoney (1922) and has since been confirmed repeatedly. Bozler (l945) recorded the electrical potentials of the dog, cat and guinea pig stomachs by means of non-polarizable differential electrodes. In the dog, the differential potential associated with each peristaltic contraction showed three main deflections, designated the R, S and T waves. The shape of the recorded potential was identical with that of cardiac muscle but differed from it in that it lasted from 5 to 8 seconds, i.e. it had a slow phase. Species differences were noted; in the guinea pig stomach a slow potential could be observed only in the region of the pylorus. In the cat the same action potentials as in the dog were obtained as long as the contractions in the stomach were weak. If movements were strong enough to be easily visible, brief spike potentials were superimposed on the slow phases; the number and frequency of the spikes increased with the strength of the contraction. At that time the significance of the spikes was not known.

Bass et al. (l96l) found that a rhythmic electric complex could be recorded regularly from the "antrum" in dogs. Called the basic electric rhythm (BER), its frequency was about 4.4 per minute. Bursts of relatively rapid changes in potential, fast or spike activity, occurred in association with approximately 40 percent of BER complexes. (In the duodenal bulb a similar basic electric rhythm and fast or spike activity was recorded.) Both types of activity became attenuated at the pylorus and usually disappeared in it. Although some of the fast activity of the antrum occasionally extended into the pylorus, it was felt that in the dog the pylorus acted as an "electric insulator" between the stomach and duodenum.

Daniel and Chapman (l963) pointed out that all investigators had recorded a more or less constant electrical wave in vitro from the body and "antrum" of both the resting and the contracting stomach. Its frequency varied from 3 to 6 per minute, depending on the species and the type of preparation. In the contracting stomach an electrical wave, which they called the primary wave, preceded each peristaltic contraction. In the dog's stomach these propagated electrical waves did not vary in shape with the presence or absence of motor activity. It was concluded that the electrical activity of the dog stomach preceded and appeared to control the spread of peristaltic contractions, but went on relatively unchanged in the absence of peristalsis.

Daniel and Chapman (l963) also investigated the electrical activity of the dog stomach by means of a monopolar technique. When the electrodes were oriented transversely to the longitudinal muscle fibres, the primary waves with a frequency of 3 to 6 per minute were the most prominent and consistent feature. In the upper third of the stomach the typical electrical wave was small and disappeared near the fundus. Activity progressed distally along an array of electrodes parallel to the greater curvature, at a velocity increasing from 0.3 cm per second in the body of the stomach to 3.0 to 4.0 cm per second as the wave neared the antrum, thus correlating electrical events with descriptions of a rapid spread of peristalsis in the antral region. Activity at the antral electrodes was often nearly simultaneous. In the antrum, but not in the body of the stomach, the primary wave was often followed by secondary smaller deflections which were sometimes fused; these were present only when visible, active peristalsis was evident. Visible antral peristaltic contractions followed the primary waves by 6 to 9 seconds and the secondary waves by 1 to 2 seconds. Daniel and Chapman (l963) described the events as follows: an electrical wave, probably originating in the cardia, travelled slowly down the stomach at a velocity of slightly more than 0.5 cm/sec until it reached the pyloric "antrum", where its velocity increased to 4 cm/sec. The wave recurred periodically at the same frequency of 3 to 6 per minute as the contractions of the stomach, and appeared to precede and initiate gastric motility. However, there was a variable relationship between electrical and mechanical events, as the primary electrical wave might continue unchanged after inhibition of motility. In the "antrum" of the dog secondary spikes accompanied motility and disappeared with it. Secondary spikes could only be recorded in the antral part of the dog's stomach, while in the cat and guinea pig stomach they occurred in the cardia.

Daniel (l965) studied the drug responses of the "antrum" and duodenal bulb in the dog, using intra-arterial infusions of drugs and combined recordings of electrical and mechanical activity. In the inactive antrum an electrical rhythm of 4 to 5 waves per minute occurred, resembling the QRS complex in the heart, and called the initial potential. It was propagated distally over most of the antrum at a velocity of 0.3 to 1.0 cm per second, but at a distance of 2.0 to 4.0cm from the pylorus the velocity increased, reaching 2.0 to 4.0 cm per second in the terminal two centimeters of the antrum; the amplitude also increased near the pylorus. In the active or contracting antrum, the above repetitive initial potential was followed by a second potential, consisting of repetitive negative going spikes in the terminal two centimeters; they did not appear to be propagated.

Daniel (l965) showed that infusion of adrenaline or noradrenaline caused inhibition of antral second potentials and contractions. Intra-arterial infusion of acetylcholine and nicotine led to the production or enhancement of second potentials and contractions; in addition, premature initial potentials might be produced and these were often propagated in an antiperistaltic direction. In the duodenum, slow waves occurred at a rhythm of l7 to l9 per minute, irrespective of mechanical activity; when contractions occurred they were preceded by a series of fast spike potentials. Acetylcholine and other cholinergic stimulants produced or increased fast spikes and contractions in the duodenum. Atropine prevented all the excitatory effects of acetylcholine and other cholinergic stimulants in both the antrum and duodenum. Bortoff and Weg (l965) studied the relationship between antral and duodenal slow waves at the gastroduodenal junction. Using feline anatomical preparations, they confirmed that spontaneous electrical activity of the pyloric "antrum" consisted of periodic depolarizations; these antral slow waves could be associated with spike potentials which were thought to initiate contractions. There was an extension of antral slow waves across the pylorus into the proximal duodenum; consequently muscular contractions initiated in the antrum could extend into the duodenum, thereby co-ordinating the activities of the antrum, pylorus and duodenal bulb. Although the results were not as definite in the dog as in the cat, they differed from those of Bass et al. (l961), who had concluded that the pylorus acted as an electric insulator, separating the electrical activity of the stomach from that of the duodenum. Bortoff and Weg (l965) found that extension of antral slow waves into the proximal duodenum could be eliminated by a transverse incision through the musculature at the gastroduodenal junction, the mucosa and submucosa being left intact; this indicated that continuity of the gastroduodenal musculature was a necessary condition for transmission of antral slow waves into the proximal duodenum. It was surmized that electrical slow waves were generated by longitudinal muscle cells; they could be recorded in the stomach in the absence of any apparent mechanical activity.

Carlson et al. (l966) simultaneously recorded intraluminal pressures, intramural electrical activity and contractions as seen cineradiographically, in fasted dogs. In the gastroduodenal junctional zone the electrical activity consisted of cyclic changes in potential, recognized as BER of the antrum, and occurring at a rate of 5.1 per minute. Between rhythmic antral BER complexes, elevations with superimposed rapid spike activity, also described as "fast activity", occurred. The presence or absence of motor activity did not affect the frequency of antral BER cycles, but did affect the contours. Motor action was associated with spike configurations; in every instance of cineradiographically identified contraction, the electric record showed associated spike activity. According to Carlson et al. (l966), a recognizable interval usually elapsed between the appearances of BER complexes at separate electrodes in the upper part of the stomach. The mean velocity of the conduction of a BER complex increased as it approached the pyloric "canal". In the body of the stomach there was a slow propagation of 0.5 cm per second, increasing to about 2.0 cm per second in the antrum. In the terminal three centimeters of the antrum simultaneous or nearly simultaneous BER complexes were recorded from different electrodes; this was consistent with the development of a simultaneous or nearly simultaneous contraction of the entire terminal antrum as seen at cineradiography.

Motor activity in the pyloric "canal", as in the antrum, was associated with fast activity in the electrical record, and occurred with the same frequency and rhythm as the fast activity in the adjacent antrum. Contraction of the pyloric canal occurred simultaneously with, or shortly after, the onset of a terminal antral contraction (TAC). (Comment: The pyloric canal was equated with the pyloric aperture). The electrical activity in the proximal duodenum was characterized by cyclic changes in potential, with a mean rate of l7.2 per minute, designated BER of the duodenum. Duodenal contractions occurred synchronously with the BER, but their precise timing with reference to contractions in the adjacent pyloric canal was irregular; BER of the stomach and duodenum did not appear to be in phase.

Although the technique of obtaining electrical records from cutaneous electrodes, called electrogastrography, had been known for a number of years, it was further developed by Nelson and Kohatsu (l968). These authors defined the slow wave in the stomach as a controlled, rhythmic, regularly propagated, moving annulus of electrical depolarization travelling from the cardia to the pylorus, and accelerating during its passage; it could be viewed as a conducted action potential. When mechanical or contractile waves were present, the electrical and mechanical waves were synchronous. The relationship of peristaltic to electric waves could be considered as locked in time but graded in amplitude from no coupling (i.e. a mechanically quiescent stomach) to complete coupling (i.e. a peristaltic wave of maximum amplitude synchronous with each electrical wave). There was a 1:1 time relationship of the peristaltic and electrical waves. In human subjects studied by means of surgical implantation of stainless steel electrodes directly into the muscle, it was found that the rate in the fasting stomach was 3 ± 0.4 cycles per minute.

Daniel and Irwin (l968) pointed out that muscular contractile activity in the stomach was rhythmic and propagated in a well co-ordinated way. Rhythmic contractions in unanaesthetized man recurred at a mean frequency of 3 per minute and in the dog at 5 per minute. Regular, propagated electrical activity was associated with this regular contractile activity. The rhythm of the elctrical activity was the same whether the stomach was contracting or inactive; during contractile activity, a second electrical component appeared. In the inactive stomach the rhythmically occurring electrical complex, previously called the basic electric rhythm (BER) or pacesetter potential, was termed the "initial potential" or "initial polarization" by Daniel and Irwin (l968). It seemed to commence some 15 to 20 cm above the pylorus in human subjects and was normally propagated toward the pylorus; both the size and the rate of propagation of the initial potential increased as it progressed. In the anaesthetized dog it had a propagation velocity of 0.1 to 0.2 cm per second near its origin, increasing to 1.5 to 4.0 cm per second in the antrum. The same general scheme had been noted previously by Carlson et al. (l966). According to Daniel and Irwin (l968) the more rapid spread of electrical activity over the antrum presumably provided the mechanism responsible for its behaviour as a motor unit.

In the active or contracting stomach, a second electrical deflection occurred, corresponding in time to the mechanically recorded contractile activity. This had previously been called "spiking potentials", "fast activity" or "action potential"; Daniel and Irwin (l968) suggested the term "second potential". It was phased by the initial potential and was typically recorded as a prolonged negative deflection, or as a series of negative spikes. Spikes were usually seen only in the terminal 2.0 or 3.0 cm of the dog antrum.

Abolishing contractile activity with moderate doses of catecholamines or atropine was associated with disappearance of the second potential according to Daniel and Irwin (l968). Activation of contraction in a previously inactive stomach resulted in the reappearance of second potentials. Thus it appeared that second potentials were associated with, or initiated, the contractile process. The second potential, unlike the initial potential, was not propagated; it could be produced locally by the local intra- arterial infusion of acetylcholine, without appearing at electrodes a few millimeters distant in either direction. It was surmized that the second potential as well as its associated contractile activity might be produced or affected by local release of chemical mediators or neurohormones, i.e. it appeared to be under local control. Daniel and Irwin (l968) found that rhythmic duodenal electrical activity in dogs, recurring at a rate of l7 per minute, existed within one millimeter of rhythmic gastric electrical activity recurring at a rate of 4.3 to 5.1 per minute. There was a possibility of coupling between the gastric and duodenal electrical rhythms since the frequency of the two rhythms could indicate a 3:1 or 4:1 coupling. These authors did not agree with Bass et al (l961) that the stomach and duodenum were electrically insulated by an interposed electrically silent zone; such insulation could only be achieved by a continuous lipid membrane, and no such structure existed at the gastroduodenal junction.

Bortoff and Davis (l968) instituted in vivo animal studies to determine whether or not transmission of slow waves across the gastroduodenal junction occurred, to study the effect of myenteric denervation on slow wave transmission and to observe the effects of vagal and splanchnic nerve stimulation. Using suction electrodes applied to the serosal surface in cats, dogs, rhesus monkeys and baboons, it was shown that "antral" slow waves spread across the junction into the proximal duodenum, where they periodically augmented depolarizations of duodenal slow waves, thereby increasing the probability of duodenal spiking. After functional myenteric denervation the duodenal spread of antral slow waves continued, indicating that it was a myogenic process; this probably occurred via bundles of antral longitudinal muscle extending across the pylorus and interdigitating with duodenal longitudinal musculature. (Comment: Some longitudinal muscle fibres normally extend across the pylorus from the stomach to the duodenum as described in Chapter 3). However, the spread could be modulated neurologically; vagal stimulation increased both amplitude and duration of antral slow waves, augmenting depolarization on both sides of the junction and increasing spike activity. Thus duodenal spiking was temporally related to antral slow waves. Splanchnic stimulation had mixed effects, causing either excitation similar to that of vagal stimulation, or inhibition of antral slow waves. It appeared if the spread of antral slow waves into the proximal duodenum constituted the primary mechanism for co-ordination of the mechanical activity at the gastroduodenal junction.

Kwong et al (l970) studied the electrical activity of the gastric "antrum" up to 6.0 cm from the pylorus in 56 patients with upper gastrointestinal pathology, and in 12 patients with gall-stones acting as controls; at operation electrodes were implanted through the serosa and others attached to the mucosa by means of suction. The same frequency was recorded from the mucosal and serosal electrodes and the main components of the wave forms were the same. In the control patients the wave frequency was approximately 3 per minute, which was significantly less than the frequency in patients with gastric ulceration, duodenal ulceration and gastric carcinoma. The general pattern of the wave forms was the same in all groups, although areas replaced by tumor were electrically silent. It was concluded that while there were differences in frequency, no differences in the pattern of electrical activity appeared which might be of diagnostic significance in these conditions.

Duthie et al. (l97l) studied the pacesetter potential in the stomach and duodenum in patients undergoing cholecystectomy. Electrodes were implanted under the serosa in the gastric "antrum" and in the duodenum as far as the duodenal papilla, the indifferent electrode being placed on the skin of the abdomen. The frequency and amplitude of the electrical waves were measured, and where possible also the conduction times. In the antrum the frequency of the pacesetter potential was stable during recordings made at rest. The waveform was similar to that obtained from electrodes sucked on to the mucosa as found by Kwong et al. (l970), and the mean frequency of about 3.12 cycles per minute was also similar. Action potentials were seen only occasionally in the unstimulated stomach. In the duodenum, from 10 to 12cm distal to the pylorus, the frequency of the pacesetter potential was about 12 cycles per minute. In the proximal 4.0 to 5.0 cm of the duodenum, the predominant pattern consisted of 3 cycles/min as in the antrum, occasionally superimposed on 12 cycles/min. However, no direct relationship could be established between the frequency of the gastric (3 cycles/min) and duodenal (12 cycles/min) intrinsic activities. The conduction velocity of the electrical waves in the antrum between 4.0 and 1.5 cm from the pylorus was about 0.5 cm per second. Across the pyloric region it was approximately 2.0cm per second, i.e. about four times as fast.

Ingestion of water, citrate or oleate significantly slowed the frequency of the pacesetter potential in the "antrum"; the injection of morphine was followed by an increase in action potentials both in the antrum and the duodenum. Duthie et al (l97l) concluded that the 3 cycles/min rhythm of the antrum passed into the proximal duodenum, but they were not able to detect any relationship between this frequency and the intrinsic 12 cycles/min frequency of the remainder of the duodenum. The route of conduction from the stomach to the duodenum was probably via the longitudinal muscle fibres continuing from the antrum across the pylorus.

Sarna (l975) suggested that the inherent rhythmic myoelectrical activity of the stomach should be termed electrical control activity. When motor activity was present, the electrical control activity was accompanied by a second component with or without superimposed fast oscillating potential changes, for which he suggested the appellation electrical response activity.

El-Sharkawy et al. (l978) simultaneously recorded mechanical and intracellular electric activity from canine and human gastric musculature, and found regional differences in the electrical signal that caused contractions. Phasic contractions in the "terminal antrum" were initiated by spike potentials whereas phasic contractions in the corpus and orad antrum were regulated by the plateau potential.

Smout et al. (l980) called the first kind of electrical activity, i.e. the omnipresent periodic activity that is not indicative of contractile activity, the electrical control activity (ECA). Electrical response activity (ERA) only occurs in connection with phasic contractile activity, but is time-locked to ECA; it does not always consist of spikes. ERA may be absent, as in the motor quiescent phase of the interdigestive myoelectric complex. According to Szurszewski (l98l) a phasic gastric contraction is usually a mechanical manifestation of an electrical event occurring in smooth muscle cells. A spontaneous electrical signal originates in the musculature of the midcorpus, which can be identified as a pacemaker region. The signal complex is propagated circumferentially around the stomach and longitudinally to the gastroduodenal junction. In canines intracellularly recorded action potentials from antral circular musculature, in the region extending from the intermediate sphincter to the gastroduodenal junction, distinguishes it from more orad regions of the stomach; similar features were likely to exist in human musculature. (Comment: The intermediate sphincter is synonymous with the left pyloric loop as described in Chap. 3). The "antrum" can be divided into orad and terminal parts, according to Szurszewski (l98l). In the corpus and proximal antrum the electrical wave forms are the same, and coincide closely with contraction of the circular muscle fibres; in the terminal 2.0 to 3.0 cm of the antrum, characteristic electrical activity is seen during contraction. The action potential in this region has an initial, rapid depolarization and a plateau potential with oscillations in potential superimposed on the plateau potential.

Stoddard et al. (l98l) reiterated that gastric myoelectric activity is characterized by the presence of regular slow waves in the distal two-thirds of the stomach, the orad third being an electrically silent area. The mean slow wave frequency is species dependent, being approximately 3 cyles per minute in man and 5 cycles per minute in dogs, with little day to day variation. The rhythm is normally remarkably stable, with only occasional irregularities of a few cycles' duration.

You and Chey (l984) pointed out that it had not been clarified whether or not a slow wave (pacesetter potential or PSP) per se was associated with a mechanical contraction. A prevailing view was that gastric contractions resulted from the occurrence of spike activity (action potential), and not from the slow wave alone; the function of the slow wave was considered to consist of setting the pace and direction of gastric contractions. However, some authors had reported an intimate relationship between contractile activity and PSP in the canine stomach, whether spike activity was present or not; a similar relationship had been found in human antral muscle segments (You et al. l980). These observations suggested that PSP in the stomach might also promote phasic contractions. In a study of the relationship between electrical and mechanical activities of the "distal antrum" in humans and canines, it was found that phasic contractions were recorded by sensitive ministrain gauges implanted on the serosal surface, although electrical activity showed only PSP's without action potentials or second potentials. (The distal antrum was defined as the region 2.0 cm proximal to the pylorus). Intraluminal manometry could not always recognize these phasic contractions; the number of contractions recorded by manometry was less than 50 percent of the PSP's accompanied by action potentials or second potentials. No gastric contractions were recorded when pacesetter potentials occurred without action potentials.

You and Chey (l984) found that gastric dysrhythmia, including tachygastria, could be induced by epinephrine. During dysrhythmia phasic contractions disappeared and no contractions occurred in association with action potentials. Tachygastria was considered to be present when PSP occurred regularly in a frequency of more than 7 cycles per minute; bradygastria indicated a frequency of less than 3 cycles per minute. Because of the insensitivity mentioned above, intraluminal manometry might not be able to detect gastric dysrhythmia.

Geldof et al. (l986) reiterated that gastric myoelectric activity could be recorded by peroral (suction) electrodes, by serosal electrodes placed at laparotomy, and by electrodes attached to the abdominal skin (electrogastrography). In a series of patients with unexplained nausea and vomiting, these authors recorded abnormal myoelectric activity by means of electrogastrography in almost 50 percent; the abnormal recordings were characterized by instability of the gastric pacemaker frequency, tachygastrias and absence of the normal increase in amplitude in the postprandial recording.

Discussion #

Periodic, rhythmic electrical activity, propagated in an aboral direction, occurs in the musculature of the stomach in man and other higher vertebrates. These waves, consisting of cyclical changes in potential, are variously known as primary waves, basic electrical rhythm (BER), slow waves, initial potential, pacesetter potential (PP) and electrical control activity (ECA). The waves occur at a rate of approximately 3 per minute in man and 6 per minute in dogs. They are omnipresent, precede and control the spread of peristalsis (Daniel and Chapman l963), but continue unchanged in the absence of peristalsis and do not indicate contractile activity.

Bursts of relatively rapid changes in potential, variously known as secondary waves, fast or spike potentials, second potential, fast activity, action potentials and electrical response activity (ERA), occur in association with some BER complexes. They are not propagated, appear to initiate contractions, and are associated with motor action.

A number of authors demonstrated a velocity increase in BER from approximately 0.3 cm per second in the corpus of the stomach to 3.0 or 4.0 cm per second in the terminal two to three centimeters of the "antrum", both in dogs (Daniel and Chapman l961, l963; Carlson et al. l966) and in man (Daniel and Irwin l968; Duthie et al. l97l). This corresponded to a "rapid spread of peristalsis" in, or "a nearly simultaneous contraction" of the terminal antrum. According to Daniel and Irwin (l968) the more rapid spread of electrical activity over the "terminal antrum" presumably provided the mechanism responsible for its behaviour as a motor unit.

The rapid progression of BER in the "terminal antrum" probably also points to some distinguishing feature or specialization of the musculature in this region. It is surmized that it is linked to the specialized musculature of the pyloric sphincteric cylinder described by Cunningham (1906), Forssell (1913) and Torgersen (l942), with its typical motor activity as discussed in Chapters 3, 13 and 15. ## References

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