Comprehensive Physiology Wiley Online Library

Esophageal motility

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Overview of Esophageal Motor Function
1.1 General Anatomy
1.2 Innervation of Esophagus and Sphincters
1.3 Deglutition Reflex
1.4 Methods of Study
2 Upper Esophageal Sphincter
2.1 Anatomy
2.2 Pressure Profile
2.3 Control of Upper Esophageal Sphincter
3 Esophageal Body
3.1 Muscular Anatomy
3.2 Pressure Profile
3.3 Central Control of Esophageal Peristalsis
3.4 Peripheral Control of Esophageal Peristalsis
3.5 Peripheral Control of Peristalsis in Esophageal Smooth Muscle
3.6 Peristalsis in the Junctional Zone
3.7 Role of Longitudinal Muscle Layer and Muscularis Mucosa in Peristalsis
4 Lower Esophageal Sphincter
4.1 Muscular Anatomy
4.2 Pressure Profile
4.3 Genesis of Basal Sphincter Pressure
4.4 Genesis of Lower Esophageal Sphincter Muscle tone
4.5 Modulation of Resting Pressure in Lower Esophageal Sphincter
4.6 Reflex Relaxation of Lower Esophageal Sphincter
4.7 Neurotransmitters of Inhibitory Pathways to Lower Esophageal Sphincter
4.8 Reflex Contractions of the Lower Esophageal Sphincter
Figure 1. Figure 1.

Primary peristalsis as recorded by intraluminal manometry. Between swallows, pharynx reflects atmospheric, esophageal intrapleural, and stomach intra‐abdominal pressures. Upper and lower esophageal sphincters (UES and LES) are identified as high‐pressure zones. Swallowing causes a rapidly propagated, short‐duration pharyngeal contraction coincident with abrupt relaxation of the UES, which is followed by postrelaxation UES contractions. Esophageal body shows peristaltic contraction that causes an aborally migrating pressure wave. The LES relaxes within 1–2 s of onset of swallowing and remains relaxed until esophageal pressure wave has reached distal esophagus; this usually takes 5–10 s. Lower esophageal sphincter pressure then recovers and a postrelaxation contraction occurs in upper part of sphincter in continuity with esophageal contraction. Duration of esophageal contractions increases distally. Contraction amplitude is greatest in pharynx and greater in distal smooth muscle esophagus than in proximal striated muscle esophagus. In the transition zone, where both striated and smooth muscle coexist, contraction amplitudes are the least. Propagation velocity of esophageal peristaltic wave increases in mid‐esophagus and then slows to its lowest level distally. Swallowed food bolus is propelled ahead of peristaltic contraction.

Figure 2. Figure 2.

Simultaneous manometric and electromyographic recordings from opossum UES. Sphincter pressure (UESP) falls abruptly on swallowing, and this is associated with cessation of tonic electrical spike activity in cricopharyngeus (CP) and inferior pharyngeal constrictor (IPC) muscles. Sphincter pressure then recovers and actually rises to well above base line (postrelaxation contraction). This corresponds to increased spike‐burst activity in CP and IPC.

From Goyal and Cobb 218
Figure 3. Figure 3.

Effect of transecting motor nerves to UES on resting pressures and deglutitive responses as evoked by superior laryngeal muscle (SLN) stimulation. During control period (A), resting UES pressure (UESP) is ∼30 mmHg. Stimulation of SLN causes initial transient UES contraction, which is followed by relaxation on activation of deglutition reflex (arrow). After sectioning motor nerves to UES (B), resting UES pressure falls to ∼10 mmHg and deglutition, which is induced by SLN stimulation, causes a further drop in pressure. Drop is due to opening of UES by contraction of suprahyoid muscles.

From Asoh and Goyal 12
Figure 4. Figure 4.

Effect of geniohyoid muscle contraction on UES pressure (UESP) in possum. Electrical stimulation of a branch of hypoglossal nerve (HGN) to geniohyoid muscle causes contraction of the muscle and precipitous fall in UES pressure. This indicates that the suprahyoid muscles function to open UES independent of relaxation of the intrinsic UES muscles.

From Asoh and Goyal 12
Figure 5. Figure 5.

Diagrammatic representation of deglutitive inhibition. Swallows taken in rapid succession are marked by repeated phasic pressure changes recorded in pharynx. The UES relaxes and recovers with each swallow on a one‐to‐one basis. However, peristalsis in esophageal body does not ensue until after last swallow. Also, the LES relaxes to first swallow and does not recover until after peristaltic wave initiated by last swallow has traversed the esophagus.

Figure 6. Figure 6.

Schematic representation of esophageal peristaltic contractions as evoked by swallowing and vagal efferent nerve stimulation. Swallowing evokes an aborally directed series of contractions that pass smoothly from striated to smooth muscle segment. Electrical stimulation of distal cut end of a vagus nerve, which simultaneously activates all vagal efferent fibers, evokes peristaltic contractions only in smooth muscle segment of esophagus. In striated muscle esophagus, vagal stimulation causes simultaneous contractions that occur only during period of stimulation. Striated muscle esophagus is dependent on central neuronal sequencing for its peristaltic contraction, whereas intrinsic neuronal mechanisms are capable of producing peristaltic sequence in smooth muscle segment.

Figure 7. Figure 7.

Swallow‐evoked discharges in 2 vagal efferent fibers, A and B. Upper trace, mylohyoid electromyographic (EMG) activity that marks the onset of deglutition (vertical line). Latency of evoked vagal efferent action potentials is short in A (0.21 s) as compared with B (1.78 s). Short‐latency fibers appear to correspond to deglutitive inhibition and long‐latency fibers to peristaltic contraction.

From Gidda and Goyal 200
Figure 8. Figure 8.

Effect of long‐train (8 s) vagal efferent nerve stimulation on esophageal contractions in opossum. Stimuli of low frequency and short pulse duration (left panel) evoke contractions during stimulus or A waves. Vagal stimulation with high frequency and longer pulse duration evoke only end‐of‐stimulus contractions or B waves (right panel). Intermediate stimulus parameters (center panel) evoke both A and B waves. Note that speed of propagation of A waves is significantly less than that of B waves and is closer to speed of swallow‐evoked peristalsis. Pharmacologic studies indicate that the A waves are mediated by cholinergic neurons whereas neurons mediating B waves are noncholinergic and nonadrenergic.

From Dodds et al. 147
Figure 9. Figure 9.

Main patterns of contraction seen with transmural electrical stimulation of opossum esophageal circular smooth muscle strips. Stimulus train duration and pulse width were constant at 10 s and 1 ms, respectively. In A, stimulus of 60 V and 40 Hz resulted in only an on contraction, occurring shortly after onset of stimulus. In C, 80 V and 10 Hz evoked only an off contraction occurring after termination of stimulus. In B, 80 V and 20 Hz produced both on and off contractions. On contractions were sensitive to cholinergic blockade with atropine, whereas off contractions were not sensitive to cholinergic or adrenergic blockade.

Adapted from Crist et al. 111
Figure 10. Figure 10.

Latencies of on (•) and off (◯) contractions of circular smooth muscle strips from different esophageal sites. Latencies of on contractions gradually increase along esophagus in an aboral direction, whereas latencies of off contractions showed no significant change along esophagus. Points, represent mean of 6 on and 8 off contractions. Electrical field stimulation parameters consisted of 80 V, 40 Hz, 1‐ms pulse duration and 10‐s train duration.]

From Crist et al. 111
Figure 11. Figure 11.

A: effect of various stimulus frequencies on latencies of contraction of circular smooth muscle strips at different sites along opossum esophagus. Increasing stimulus frequency from 2 Hz (◯) to 40 Hz (▴) resulted in decrease in latencies of contraction at more proximal sites (11, 9, and 7 cm above LES) and increase in latencies of contraction at more distal sites (5, 3, and 1 cm above LES). B: effect of increase in stimulus frequency 2,5,10,20, and 40 Hz) on latencies of contraction of circular smooth muscle strips from sites 11 and 1 cm above LES. At 1‐cm site, there is a progressive increase in latency of contraction with increases in stimulus frequency. At the 11‐cm site, increasing stimulus frequency resulted in a decrease in latencies of contraction. This is due to stimulation of cholinergic neurons in the proximal esophagus.

From Crist et al. 112
Figure 12. Figure 12.

Schematic drawing illustrating gradients of cholinergic (C) and noncholinergic (NC) nerve influence along smooth muscle portion of esophagus. Cholinergic influence is most prominent proximally and progressively decreases distally, whereas noncholinergic influence is most prominent distally and progressively decreases proximally.

From Crist et al. 112
Figure 13. Figure 13.

Examples of electromechanically coupled (A) and uncoupled (B and C) responses to vagal efferent nerve stimulation (VS) as recorded by bipolar pressure electrodes in opossum distal esophageal body. A: electrical spike bursts precede pressure wave caused by esophageal contraction. B: spike burst occurs without esophageal contraction. However, spike burst is of low amplitude and has fewer spikes than the coupled responses A. C: vagal stimulation evokes contraction without electrical spike burst.

From Goyal and Gidda 219
Figure 14. Figure 14.

Example of simultaneous recording of electrical and mechanical (intraluminal pressure) events in smooth muscle opossum esophagus in response to swallowing (S). Swallowing results in prompt fall in membrane potential (hyperpolarization) that is followed by overshoot depolarization and superimposed electrical spike bursts. Esophageal contraction occurs after onset of spike burst. This provides direct evidence that deglutition results in initial inhibition of esophagus prior to peristaltic contractions.

From Rattan et al. 381
Figure 15. Figure 15.

Proposed scheme for anatomic radiologic landmarks of the lower esophageal sphincter.

From Goyal 212
Figure 16. Figure 16.

Influence of inflation of an intraluminal esophageal balloon on electrical activity and pressures of distal esophageal body and LES. Balloon inflation causes a cessation of tonic LES spike activity and simultaneous fall in LES pressure. Balloon deflation causes spike activity that precedes contraction in esophageal body; in LES, tonic spike activity reappears as LES pressure returns toward base line.

From Asoh and Goyal 11
Figure 17. Figure 17.

Schematic representation of extrinsic (vagal) and intrinsic inhibitory pathways to LES. Vagal preganglionic efferent neurons synapse with postganglionic inhibitory neurons within LES. Synaptic neurotransmitter is mainly acetylcholine and activates inhibitory postganglionic neurons by stimulating both nicotinic and muscarinic receptors. There is also evidence that serotonin may also be involved in synaptic transmission as complete pharmacologic blockade of vagally induced LES relaxation requires a combination of muscarinic, nicotinic, and serotonin antagonists. The postganglionic inhibitory neuron can also be activated by an intramural neuron (e.g., a mechanoreceptor); however, the neurotransmitter involved at this synapse is unknown. The postganglionic inhibitory neuron in turn releases a nonadrenergic, noncholinergic neurotransmitter (?VIP) that directly relaxes the LES smooth muscle.

Adapted from Goyal 212


Figure 1.

Primary peristalsis as recorded by intraluminal manometry. Between swallows, pharynx reflects atmospheric, esophageal intrapleural, and stomach intra‐abdominal pressures. Upper and lower esophageal sphincters (UES and LES) are identified as high‐pressure zones. Swallowing causes a rapidly propagated, short‐duration pharyngeal contraction coincident with abrupt relaxation of the UES, which is followed by postrelaxation UES contractions. Esophageal body shows peristaltic contraction that causes an aborally migrating pressure wave. The LES relaxes within 1–2 s of onset of swallowing and remains relaxed until esophageal pressure wave has reached distal esophagus; this usually takes 5–10 s. Lower esophageal sphincter pressure then recovers and a postrelaxation contraction occurs in upper part of sphincter in continuity with esophageal contraction. Duration of esophageal contractions increases distally. Contraction amplitude is greatest in pharynx and greater in distal smooth muscle esophagus than in proximal striated muscle esophagus. In the transition zone, where both striated and smooth muscle coexist, contraction amplitudes are the least. Propagation velocity of esophageal peristaltic wave increases in mid‐esophagus and then slows to its lowest level distally. Swallowed food bolus is propelled ahead of peristaltic contraction.



Figure 2.

Simultaneous manometric and electromyographic recordings from opossum UES. Sphincter pressure (UESP) falls abruptly on swallowing, and this is associated with cessation of tonic electrical spike activity in cricopharyngeus (CP) and inferior pharyngeal constrictor (IPC) muscles. Sphincter pressure then recovers and actually rises to well above base line (postrelaxation contraction). This corresponds to increased spike‐burst activity in CP and IPC.

From Goyal and Cobb 218


Figure 3.

Effect of transecting motor nerves to UES on resting pressures and deglutitive responses as evoked by superior laryngeal muscle (SLN) stimulation. During control period (A), resting UES pressure (UESP) is ∼30 mmHg. Stimulation of SLN causes initial transient UES contraction, which is followed by relaxation on activation of deglutition reflex (arrow). After sectioning motor nerves to UES (B), resting UES pressure falls to ∼10 mmHg and deglutition, which is induced by SLN stimulation, causes a further drop in pressure. Drop is due to opening of UES by contraction of suprahyoid muscles.

From Asoh and Goyal 12


Figure 4.

Effect of geniohyoid muscle contraction on UES pressure (UESP) in possum. Electrical stimulation of a branch of hypoglossal nerve (HGN) to geniohyoid muscle causes contraction of the muscle and precipitous fall in UES pressure. This indicates that the suprahyoid muscles function to open UES independent of relaxation of the intrinsic UES muscles.

From Asoh and Goyal 12


Figure 5.

Diagrammatic representation of deglutitive inhibition. Swallows taken in rapid succession are marked by repeated phasic pressure changes recorded in pharynx. The UES relaxes and recovers with each swallow on a one‐to‐one basis. However, peristalsis in esophageal body does not ensue until after last swallow. Also, the LES relaxes to first swallow and does not recover until after peristaltic wave initiated by last swallow has traversed the esophagus.



Figure 6.

Schematic representation of esophageal peristaltic contractions as evoked by swallowing and vagal efferent nerve stimulation. Swallowing evokes an aborally directed series of contractions that pass smoothly from striated to smooth muscle segment. Electrical stimulation of distal cut end of a vagus nerve, which simultaneously activates all vagal efferent fibers, evokes peristaltic contractions only in smooth muscle segment of esophagus. In striated muscle esophagus, vagal stimulation causes simultaneous contractions that occur only during period of stimulation. Striated muscle esophagus is dependent on central neuronal sequencing for its peristaltic contraction, whereas intrinsic neuronal mechanisms are capable of producing peristaltic sequence in smooth muscle segment.



Figure 7.

Swallow‐evoked discharges in 2 vagal efferent fibers, A and B. Upper trace, mylohyoid electromyographic (EMG) activity that marks the onset of deglutition (vertical line). Latency of evoked vagal efferent action potentials is short in A (0.21 s) as compared with B (1.78 s). Short‐latency fibers appear to correspond to deglutitive inhibition and long‐latency fibers to peristaltic contraction.

From Gidda and Goyal 200


Figure 8.

Effect of long‐train (8 s) vagal efferent nerve stimulation on esophageal contractions in opossum. Stimuli of low frequency and short pulse duration (left panel) evoke contractions during stimulus or A waves. Vagal stimulation with high frequency and longer pulse duration evoke only end‐of‐stimulus contractions or B waves (right panel). Intermediate stimulus parameters (center panel) evoke both A and B waves. Note that speed of propagation of A waves is significantly less than that of B waves and is closer to speed of swallow‐evoked peristalsis. Pharmacologic studies indicate that the A waves are mediated by cholinergic neurons whereas neurons mediating B waves are noncholinergic and nonadrenergic.

From Dodds et al. 147


Figure 9.

Main patterns of contraction seen with transmural electrical stimulation of opossum esophageal circular smooth muscle strips. Stimulus train duration and pulse width were constant at 10 s and 1 ms, respectively. In A, stimulus of 60 V and 40 Hz resulted in only an on contraction, occurring shortly after onset of stimulus. In C, 80 V and 10 Hz evoked only an off contraction occurring after termination of stimulus. In B, 80 V and 20 Hz produced both on and off contractions. On contractions were sensitive to cholinergic blockade with atropine, whereas off contractions were not sensitive to cholinergic or adrenergic blockade.

Adapted from Crist et al. 111


Figure 10.

Latencies of on (•) and off (◯) contractions of circular smooth muscle strips from different esophageal sites. Latencies of on contractions gradually increase along esophagus in an aboral direction, whereas latencies of off contractions showed no significant change along esophagus. Points, represent mean of 6 on and 8 off contractions. Electrical field stimulation parameters consisted of 80 V, 40 Hz, 1‐ms pulse duration and 10‐s train duration.]

From Crist et al. 111


Figure 11.

A: effect of various stimulus frequencies on latencies of contraction of circular smooth muscle strips at different sites along opossum esophagus. Increasing stimulus frequency from 2 Hz (◯) to 40 Hz (▴) resulted in decrease in latencies of contraction at more proximal sites (11, 9, and 7 cm above LES) and increase in latencies of contraction at more distal sites (5, 3, and 1 cm above LES). B: effect of increase in stimulus frequency 2,5,10,20, and 40 Hz) on latencies of contraction of circular smooth muscle strips from sites 11 and 1 cm above LES. At 1‐cm site, there is a progressive increase in latency of contraction with increases in stimulus frequency. At the 11‐cm site, increasing stimulus frequency resulted in a decrease in latencies of contraction. This is due to stimulation of cholinergic neurons in the proximal esophagus.

From Crist et al. 112


Figure 12.

Schematic drawing illustrating gradients of cholinergic (C) and noncholinergic (NC) nerve influence along smooth muscle portion of esophagus. Cholinergic influence is most prominent proximally and progressively decreases distally, whereas noncholinergic influence is most prominent distally and progressively decreases proximally.

From Crist et al. 112


Figure 13.

Examples of electromechanically coupled (A) and uncoupled (B and C) responses to vagal efferent nerve stimulation (VS) as recorded by bipolar pressure electrodes in opossum distal esophageal body. A: electrical spike bursts precede pressure wave caused by esophageal contraction. B: spike burst occurs without esophageal contraction. However, spike burst is of low amplitude and has fewer spikes than the coupled responses A. C: vagal stimulation evokes contraction without electrical spike burst.

From Goyal and Gidda 219


Figure 14.

Example of simultaneous recording of electrical and mechanical (intraluminal pressure) events in smooth muscle opossum esophagus in response to swallowing (S). Swallowing results in prompt fall in membrane potential (hyperpolarization) that is followed by overshoot depolarization and superimposed electrical spike bursts. Esophageal contraction occurs after onset of spike burst. This provides direct evidence that deglutition results in initial inhibition of esophagus prior to peristaltic contractions.

From Rattan et al. 381


Figure 15.

Proposed scheme for anatomic radiologic landmarks of the lower esophageal sphincter.

From Goyal 212


Figure 16.

Influence of inflation of an intraluminal esophageal balloon on electrical activity and pressures of distal esophageal body and LES. Balloon inflation causes a cessation of tonic LES spike activity and simultaneous fall in LES pressure. Balloon deflation causes spike activity that precedes contraction in esophageal body; in LES, tonic spike activity reappears as LES pressure returns toward base line.

From Asoh and Goyal 11


Figure 17.

Schematic representation of extrinsic (vagal) and intrinsic inhibitory pathways to LES. Vagal preganglionic efferent neurons synapse with postganglionic inhibitory neurons within LES. Synaptic neurotransmitter is mainly acetylcholine and activates inhibitory postganglionic neurons by stimulating both nicotinic and muscarinic receptors. There is also evidence that serotonin may also be involved in synaptic transmission as complete pharmacologic blockade of vagally induced LES relaxation requires a combination of muscarinic, nicotinic, and serotonin antagonists. The postganglionic inhibitory neuron can also be activated by an intramural neuron (e.g., a mechanoreceptor); however, the neurotransmitter involved at this synapse is unknown. The postganglionic inhibitory neuron in turn releases a nonadrenergic, noncholinergic neurotransmitter (?VIP) that directly relaxes the LES smooth muscle.

Adapted from Goyal 212
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Raj K. Goyal, William G. Paterson. Esophageal motility. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 865-908. First published in print 1989. doi: 10.1002/cphy.cp060122