Elsevier

Clinical Neurophysiology

Volume 114, Issue 12, December 2003, Pages 2226-2244
Clinical Neurophysiology

Invited review
Neurophysiology of swallowing

https://doi.org/10.1016/S1388-2457(03)00237-2Get rights and content

Abstract

Swallowing is a complex motor event that is difficult to investigate in man by neurophysiological experiments. For this reason, the characteristics of the brain stem pathways have been studied in experimental animals.

However, the sequential and orderly activation of the swallowing muscles with the monitoring of the laryngeal excursion can be recorded during deglutition. Although influenced by the sensory and cortical inputs, the sequential muscle activation does not alter from the perioral muscles caudally to the cricopharyngeal sphincter muscle. This is one evidence for the existence of the central pattern generator for human swallowing. The brain stem swallowing network includes the nucleus tractus solitarius and nucleus ambiguus with the reticular formation linking synaptically to cranial motoneuron pools bilaterally.

Under normal function, the brain stem swallowing network receives descending inputs from the cerebral cortex. The cortex may trigger deglutition and modulate the brain stem sequential activity. The voluntarily initiated pharyngeal swallow involves several cortical and subcortical pathways. The interactions of regions above the brain stem and the brain stem swallowing network is, at present, not fully understood, particularly in humans.

Functional neuroimaging methods were recently introduced into the human swallowing research. It has been shown that volitional swallowing is represented in the multiple cortical regions bilaterally but asymmetrically. Cortical organisation of swallowing can be continuously changed by the continual modulatory ascending sensory input with descending motor output.

Significance: Dysphagia is a severe symptom complex that can be life threatening in a considerable number of patients. Three-fourths of oropharyngeal dysphagia is caused by neurological diseases. Thus, the responsibility of the clinical neurologist and neurophysiologist in the care for the dysphagic patients is twofold. First, we should be more acquainted with the physiology of swallowing and its disorders, in order to care for the dysphagic patients successfully. Second, we need to evaluate the dysphagic problems objectively using practical electromyography methods for the patients' management. Cortical and subcortical functional imaging studies are also important to accumulate more data in order to get more information and in turn to develop new and effective treatment strategies for dysphagic patients.

Introduction

Swallowing is a complex sensorimotor behaviour involving the coordinated contraction and inhibition of the musculature located around the mouth and at the tongue, larynx, pharynx and esophagus bilaterally. During a swallow, different levels of the central nervous system from the cerebral cortex to the medulla oblongata are involved and many of the striated muscles innervated by the cranial nerves (CN) are excited and/or inhibited sequentially for the execution of the passage of bolus from the mouth to the stomach (Miller, 1982, Jean, 1984, Jean, 1986, Jean, 2001, Donner et al., 1985, Broussard and Altschuler, 2000a).

Swallowing has received less attention than other fundamental motor activities such as locomotion, mastication, or respiration. This is probably due to the complexity of the motor pattern along with the greater number of muscles and CN involved, which renders neurophysiological studies difficult in experimental animals and humans. Although recent advances in the evaluation of dysphagia allow for the diagnosis, prognosis, and treatment of swallowing problems, such information in human subjects does not bring much knowledge to the basic understanding of the complex physiology of deglutition (Schindler and Kelly, 2002).

Swallowing and its disorders have been intensively investigated by videofluoroscopic, manometric and endoscopic methods. These studies are especially useful for clinical problems, however, it is necessary to develop new techniques, in order to understand the central neural mechanisms controlling swallowing. This review is limited to the neurophysiology of oropharyngeal swallowing. The esophageal phase of swallowing is beyond the scope of this review.

Section snippets

Peripheral events in swallowing

It has become convenient to state that, swallowing is subdivided into 3 phases: oral, pharyngeal, and esophageal. This conventional division of the human swallowing is usually ascribed to Magendie (1825) (Miller, 1982). The swallow has, however, also been described in two stages i.e. the buccopharyngeal (or oropharyngeal) and esophageal stages (Thexton and Crompton, 1998, Jean, 2001).

The 3 phases of swallowing are probably related to their innervation pattern: the oral phase is often accepted

EMG in swallowing muscles

The sequential and orderly activity of swallowing muscles can be demonstrated by EMG methods. Considerable number of studies have been performed for swallowing muscles in experimental animals and to some extent in man.

Doty and Bosma (1956) described the pattern of EMG activity in the oral and pharyngeal muscles in dog during swallowing elicited reflexively by electrical and mechanical stimuli. The pattern of EMG activity reported in that study and others subsequently, suggests the concept of a

Brain stem and swallowing

We owe almost all our knowledge to experimental deglutition studies except some information that was generated by clinical studies. Therefore, most of the information related to the brain stem and swallowing has been obtained from non-human mammals.

The precise pattern of muscle contraction and inhibition sequentially as mentioned above is dependent on brain stem neural structures that conceptually consist of 3 levels (Broussard and Altschuler, 2000b):

  • 1.

    An afferent and/or descending input level

Cerebral cortex and voluntary swallowing

Although the act of swallowing is thought to be mediated principally by brain stem mechanisms (Jean, 2001) converging evidence from electrophysiological, neuroimaging, and clinical studies indicates that the cerebral cortex also plays a fundamental role in the regulation of swallowing (Martin and Sessle, 1993, Miller, 1999).

In animal models, particularly the non-human primate, studies employing cortical stimulation (Jean and Car, 1979, Huang et al., 1989, Martin et al., 1997, Martin et al., 1999

Conclusions

Swallowing is subdivided into 3 phases: oral, pharyngeal and, esophageal phases. The oral cavity, pharynx, and larynx are anatomically separated but functionally integrated for the complex and sequential motor responses that include chewing, swallowing and speech. From the point of swallowing, the oral and pharyngeal phases are highly interrelated and the term oropharyngeal swallowing is often used. Despite this, the oral phase is often accepted as voluntary, while the pharyngeal phase is

Acknowledgements

This work has been supported in part by the Turkish Academy of Sciences.

We are also grateful for the cooperation of our co-workers, especially Murat Pehlivan, MD, Nur Yüceyar, MD, Nefati Kıylıoglu, MD, Sultan Tarlaci, MD, Yaprak Secil, MD. We thank Nilüfer Ertekin-Taner MD, PhD, who reviewed the English text.

References (191)

  • C. Ertekin et al.

    Cricopharyngeal sphincter muscle responses to transcranial magnetic stimulation in normal subjects and in patients with dysphagia

    Clin Neurophysiol

    (2001)
  • K. Ezure et al.

    Location and axonal projection of one type swallowing interneurons in cat medulla

    Brain Res

    (1993)
  • C. Fraser et al.

    Driving plasticity in human adult motor cortex associated with improved motor function after brain injury

    Neuron

    (2002)
  • P.L. Furlong et al.

    Cortical localisation of magnetic fields evoked by esophageal distension

    Electroenceph clin Neurophysiol

    (1998)
  • R.K. Goyal

    Disorders of the cricopharyngeal muscle

    Otolaryngol Clin North Am

    (1984)
  • S. Hamdy et al.

    Explaining oropharyngeal dysphagia after unilateral hemispheric stroke

    Lancet

    (1997)
  • S. Hamdy et al.

    Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex

    Gastroenterology

    (1998)
  • P. Jacob et al.

    Upper esophageal sphincter opening and modulation during swallowing

    Gastroenterology

    (1989)
  • A. Jean et al.

    Inputs to swallowing medullary neurons from the peripheral afferent fibers and swallowing cortical area

    Brain Res

    (1979)
  • A. Jean et al.

    Connections between the medullary swallowing area and the trigeminal motor nucleus of the sheep studied by tracing methods

    J Auton Nerv Syst

    (1983)
  • P.J. Kahrilas et al.

    Upper esophageal sphincter function during deglutition

    Gastroenterology

    (1988)
  • P.J. Kahrilas et al.

    Pharyngeal clearance during swallowing: a combined manometric and videofluoroscopic study

    Gastroenterology

    (1992)
  • M.K. Kern et al.

    Identification and characterization of cerebral cortical response to esophageal acid exposure and distension

    Gastroenterology

    (1998)
  • J.P. Kessler

    Involvement of excitatory aminoacids in the activity of swallowing related neurons of the ventrolateral medulla

    Brain Res

    (1993)
  • M.L. Alberts et al.

    Aspiration after stroke: lesion analysis by brain MRI

    Dysphagia

    (1992)
  • G.N. Ali et al.

    Influence of mucosal receptors on deglutitive regulation of pharyngeal and upper esophageal sphincter function

    Am J Physiol

    (1994)
  • S.M. Altschuler

    Laryngeal and respiratory protective reflexes

    Am J Med

    (2001)
  • M. Amri et al.

    Medullary control of the pontine swallowing neurons in sheep

    Exp Brain Res

    (1984)
  • J.R. Augustine

    Circuitry and functional aspects of the insular lobe in primates including humans

    Brain Res

    (1996)
  • J.E. Aviv et al.

    Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia

    Ann Otol Rhinol Laryngol

    (1996)
  • J.E. Aviv et al.

    Silent laryngopharyngeal sensory deficits after stroke

    Ann Otol Rhinol Laryngol

    (1997)
  • I. Aydogdu et al.

    Dysphagia in lateral medullary infarction (Wallenberg's syndrome): an acute disconnection syndrome in premotor neurons related to swallowing activity

    Stroke

    (2001)
  • Q. Aziz et al.

    Cortical processing of human somatic and visceral sensation

    J Neurosci

    (2000)
  • D.H. Barer

    The natural history and functional consequences of dysphagia after hemispheric stroke

    J Neurol Neurosurg Psychiatry

    (1989)
  • N.H. Bass

    The neurology of swallowing

  • D. Bieger

    Neuropharmacologic correlates of deglutition: lessons from fictive swallowing

    Dysphagia

    (1991)
  • D. Bieger

    Rhomboncephalic pathways and neurotransmitters controlling deglutition

    Am J Med

    (2001)
  • H.A.J. Brook et al.

    Evidence for recurrent laryngeal nerve contribution in motor innervation of the human cricopharyngeal muscle

    Laryngoscope

    (1999)
  • D.L. Broussard et al.

    Central integration of swallow and airway-protective reflexes

    Am J Med

    (2000)
  • D.L. Broussard et al.

    Brainstem viscerotopic organisation of afferents and efferents involved in the control of swallowing

    Am J Med

    (2000)
  • B.P. Brown et al.

    Diagnostic methods to evaluate swallowing other than barium contrast

  • G.Z. Chiao et al.

    Neuronal activity in nucleus ambiguus during deglutition and vocalization in conscious monkeys

    Exp Brain Res

    (1994)
  • C. Chiron et al.

    The right brain hemisphere is dominant in human infants

    Brain

    (1997)
  • I.J. Cook et al.

    Opening mechanism of the human upper esophageal sphincter

    Am J Physiol

    (1989)
  • D.S. Cooper et al.

    Electromyography in the functional and diagnostic testing of deglutition

  • D.R. Corfield et al.

    Cortical and subcortical control of tongue movements in humans: a functional neuroimaging study using fMRI

    J Appl Physiol

    (1999)
  • D.P. Cunningham et al.

    Electromyography of genioglossus and geniohyoid muscles during deglutition

    Anat Rec

    (1969)
  • S.K. Daniels et al.

    The role of the insular cortex in dysphagia

    Dysphagia

    (1997)
  • S.K. Daniels et al.

    Lingual discoordination and dysphagia following acute stroke: analysis of lesion location

    Dysphagia

    (1999)
  • R.O. Dantas et al.

    Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing

    Am J Physiol

    (1990)
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