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www.elsevier.com/locate/clinph
Invited review
Neurophysiology of swallowing
Cumhur Ertekina,b,*, Ibrahim Aydogdua,b
a
Department of Clinical Neurophysiology, Ege University, Medical School Hospital, Bornova, Izmir, Turkey
b
Department of Neurology, Ege University, Medical School Hospital, Bornova, Izmir, Turkey
Accepted 23 June 2003
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.
q 2003 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Keywords: Neurophysiology; Swallowing; Deglutition; Central pattern generator; Electromyography; Functional brain mapping
1. 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
* Corresponding author. Gonc Apt. Talatpasa Bulvar, No: 12 D.3, 35220
Alsancak, Izmir, Turkey. Tel.: 90-232-4220160; fax: 90-232-4630074.
E-mail addresses: erteker@unimedya.net.tr (C. Ertekin), iaydog@ttnet.
net.tr (I. Aydogdu).
1388-2457/$30.00 q 2003 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/S1388-2457(03)00237-2
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Fig. 1. The integrated orbicularis oris (O. Oris) (top traces in each pair) and submental muscle electromyography (SM-EMG) (lower trace in each pair)
activities (surface electrodes) during swallowing of different amounts of water, increasing in quantity step by step from 3 to 20 ml. Note that all volumes were
swallowed at one go up to 20 ml in a normal adult subject (A), while, in a stroke patient with dysphagia (B), the bolus is divided into two or more separate
swallows during the swallowing of 1020 ml water. (Arrows indicate the second and subsequent swallows). The sweep duration set at 10 s and the delay line
was adjusted to O. Oris at 2 s. Amplitude calibration: 70 mV (A) and 50 mV (B). Time calibration: 1000 ms in all traces.
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Fig. 3. Thyroarytenoid EMG (rectified and integrated) activity of a normal subject with simultaneous recording of laryngeal vertical movement during
swallowing of 3 ml water. The onset of upward deflection of the larynx is denoted by 0 and that of downward by 2. Five traces were averaged in all.
Onset and End belong to basic activity (from Ertekin et al., 2000d; by permission).
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Fig. 4. Schematic representation of the central pattern generator of swallowing. Peripheral and supramedullary inputs reach to and around nucleus tractus
solitariusdorsal swallowing group (NTS-DSG). NTS-DSG activates the ventral swallowing group of premotor neurons in the ventrolateral medullaventral
swallowing group (VLM-VSG) adjacent to the nucleus ambiguus (NA). VLM-VSG drives the motoneuron pools of the V, VII, IX, X, XII, C1 3 CN bilaterally
(modified from Jean, 2001).
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6. 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 considered a reflex
response. Apart from the chewing and taste functions, the
oral phase is primarily related with the oral preparation and
the triggering to the pharyngeal phase of swallowing.
Sensory inputs arising from posterior oral, pharyngeal and
some laryngeal mucosae and transmitted to the medullary
NTS and the cerebral cortex are necessary for the triggering
of the bolus in the oropharyngeal region. Once swallowing
is initiated, the cascade of the sequential muscle activation
does not essentially alter from the perioral muscles downward. The main events are the transport of the food safely to
pharyngoesophageal segment by the activation of the
tongue, submental/suprahyoid muscles and pharyngeal
constrictor muscles and the relaxation and opening the CP
sphincter muscle. During the food transport, the airway is
protected and closed by several laryngeal muscles and the
larynx is pulled up.
The sequential and orderly activity of swallowing
muscles can be demonstrated by EMG methods. Submental/suprahyoid muscles are easily recorded by surface
electrodes and demonstrate the onset and complete duration
of the oropharyngeal phase of swallowing. Laryngeal and
pharyngeal muscles are approached by needle electrodes or
by means of intraluminar catheter electrodes. The CP
muscle of the UES is tonically active during rest and the
tonic activity ceases during a swallow.
Some premotor neurons or interneurons are found in the
bulbar reticular formation, which can initiate or organise
the swallowing motor neurons. Their network is known as
the CPG. These neurons are located in and around the NTS
and around the NA of the ventrolateral medulla oblongata.
The premotor neurons in and around NTS contain the
generator neurons involved in the triggering, shaping and
timing of the sequential swallowing pattern. The premotor
neurons around the NA contain the switching neurons which
distribute the swallowing drive to the various pools of the
motoneurons involved in swallowing (V, VII, IX, X, XII
cranial motoneurons). Anatomical connections mediated by
nerve fibers crossing the midline exist between the two
medullary regions where the swallowing neurons are
located in and around the NTS and NA.
The descending excitatory and inhibitory drives from the
cortex and subcortex influence the oropharyngeal swallowing and trigger and modulate the CPG. The cortical control
of CPG must have increased phylogenetically and reached
its maximum control in the humans.
Acknowledgements
This work has been supported in part by the Turkish
Academy of Sciences.
We are also grateful for the cooperation of our coworkers, especially Murat Pehlivan, MD, Nur Yuceyar,
MD, Nefati Kyloglu, MD, Sultan Tarlaci, MD, Yaprak
Secil, MD. We thank Nilufer Ertekin-Taner MD, PhD, who
reviewed the English text.
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