Aliment Pharmacol Ther 2013; 37(2):263–274.
5 Functional Anatomy and Physiology of Swallowing and Esophageal Motility
Arvind Rengarajan and C. Prakash Gyawali
Washington University School of Medicine, St. Louis, Missouri, USA
Introduction
The esophagus is a hollow muscular tube with sphincters at either end. The upper esophageal sphincter (UES) is formed by the fibers of the cricopharyngeus, a skeletal muscle that is contiguous with pharyngeal muscles proximally, and the striated muscle in the proximal esophagus distally. The transition between skeletal muscle in the proximal esophagus and smooth muscle in the distal esophagus occurs in the proximal third of the tubular esophagus. The lower esophageal sphincter (LES) is formed entirely of smooth muscle. The main functions of the esophagus are to transport ingested content from the pharynx into the stomach, and to clear noxious gastric content refluxed into the esophagus. Esophageal motor function includes esophageal primary and secondary peristalsis, esophageal shortening, and esophageal tone. These functions are dependent on control mechanisms, both peripheral and central, interrelated with oral and pharyngeal function, airway function, gastric function, as well as relationships to other intrathoracic organs, both central and peripheral. Both motor and sensory pathways exist between the esophagus and the central nervous system, which interface with ganglia and postganglionic nerves located in between circular and longitudinal muscle layers of the esophagus.
The esophagus is unique in its anatomy and physiology. The swallowing process combines volitional central control mechanisms with involuntary/reflex controls, both central and peripheral. The esophagus transits through cavities of different pressures, from atmospheric pressure at the mouth, to negative intrathoracic pressure, to positive intra‐abdominal pressure, with sphincters separating pressures and organ contents in each cavity. The sphincters open temporarily to allow the passage of food aborally and air and gastric contents orally with belching and vomiting.
Understanding of central and peripheral control mechanisms for swallowing, and particularly esophageal function, derives from animal experimentation. Since species can differ in physiologic mechanisms, application of animal findings to human physiology may not be perfect and needs to be kept in mind. Studies of central mechanisms are derived from animals with a totally striated muscle esophageal body (such as the sheep, rat, mouse, ferret, and dog). The LES is composed of smooth muscle in all species. Studies in species with a significant portion of the esophageal body composed of smooth muscle, such as the opossum, cat, and to a lesser extent the non‐human primate and humans, have provided a large amount of information about the peripheral control mechanisms in the smooth muscle esophageal body and LES.
Swallowing
A swallow can be initiated by volition during eating or drinking. However, swallows also occur involuntarily, when saliva or respiratory secretions accumulate in the pharynx [1]. Sensory information for initiation of reflexive swallows is transmitted through the superior laryngeal, glossopharyngeal, and recurrent laryngeal nerves [2]. Swallowing occurs about 600 times a day, mainly while awake and during eating, and to a lesser extent (50 swallows) while asleep [3]. Central control of striated muscles in the oropharynx, UES, and upper esophagus is integrated with intrinsic control mechanisms in the distal smooth muscle esophagus and the LES. In both locations, sensory information is integrated with motor function such that swallowing seamlessly follows mastication and propulsion of the bolus into the pharynx.
Swallowing pattern generator
Swallowing is controlled by a network of neurons in the brainstem that form a swallowing pattern generator (SPG), which can produce sequential and rhythmic motor activity [4]. The SPG has complex connections to higher regions in the midbrain and the cerebral cortex and to the motor nuclei of cranial nerves serving over 50 different muscles along the swallowing pathway. Peripheral sensory input from the mouth, pharynx, and esophagus feed into the SPG and modulate its response to the nature of the bolus ingested. The SPG can be activated by cortical input when a swallow is voluntarily initiated, or triggered by peripheral sensory input in a reflexive swallow or secondary peristalsis. Thus, the SPG programs sequential motor output to the muscles along the entire swallowing pathway.
The SPG is not a single unit. Three functional stages of voluntary swallows – oral, pharyngeal, and esophageal – occur in sequence to move the bolus out of the mouth, through the pharynx and into the esophagus [5]. Each functional stage has its own central pattern generator within the SPG; these are linked together with each stage activating the next [6]. The SPG and its components are essential for a number of coordinated physiologic functions: (i) efficient propulsion of the bolus through the entire swallowing pathway; (ii) elevation of the larynx and closure of the laryngeal inlet for airway protection; (iii) initiation of peristalsis at the pharynx or different levels in the esophagus independent of voluntary swallowing; (iv) contraction and relaxation of the UES and LES; (v) deglutitive and distal inhibition; and (vi) coordination with reflexes connecting swallowing to respiratory, cardiovascular, and gastrointestinal physiology.
Organizational structure and function
The structure of the SPG consists of sensory input into a programming circuitry of neurons and a group of appropriate motor neurons [7]. There are two groups of neurons with specific functions in the programming circuitry (Figure 5.1): (i) the dorsal swallowing group (DSG), located in the nucleus of the solitary tract (NTS) and adjacent dorsal medullary reticular formation, responsible for generation and timing of swallow related events; and (ii) a ventral swallowing group (VSG), a collection of interneurons within the ventral reticular formation dorsomedial to the nucleus ambiguus, which function as a switching station for signals from the DSG to motor neurons of cranial nerves innervating muscles in the swallowing pathway [2]. Input from higher centers such as the cortex feed into each stage of the SPG. Bilateral connectivity occurs at the level of the NTS; additionally, the DSG and VSG are connected either directly or through interneurons. Sensory feedback from the periphery modulates the activity of the programming circuitry.
Figure 5.1 Central control of the oropharynx and esophagus. The oropharyngeal circuitry is shown on the left and the esophageal on the right. Both have a dorsal swallowing group (DSG) in the solitary tract nucleus for programming and organizing the sequential events in their respective locations. The oropharyngeal DSG leads the esophageal DSG. The oropharyngeal mechanism has a ventral swallowing group (VSG) in the ventral lateral medulla where “switching” of the DSG signaling distributes excitation to the appropriate cranial nerves for the mouth, pharynx, and larynx. The esophageal circuit likely has a VSG but may be simpler, with a direct connection from the DSG to the motor nuclei. Both circuits can receive inputs from the periphery, the cerebral cortex, and various supramedullary structures. DMX, dorsal motor nucleus of the vagus; NA, nucleus ambiguus.
Source: Jean [7] with permissions of Springer Nature.
Sensory
Several cranial nerves participate in sensory feedback for the oropharyngeal stages of swallowing, including trigeminal (especially maxillary branch), facial, glossopharyngeal, and vagus [8–12]. Sensory initiation of the pharyngeal phase of swallowing occurs through the superior laryngeal nerve (SLN) of the vagus nerve [5, 9]. The pharynx is highly sensitive; as little as 0.5 mL of fluid injected quickly into the pharynx can initiate human swallowing [13–15]. Esophageal feedback occurs via the vagus nerve with its cell bodies