Neural control of swallowing

REVIEW

Arq Gastroenterol • 2018. v. 55. Suplemento • 61

Milton Melciades Barbosa COSTA

Received 11/4/2018

Accepted 9/5/2018

ABSTRACT – Background – Swallowing is a motor process with several discordances and a very difcult neurophysiological study. Maybe that is the

reason for the scarcity of papers about it. Objective – It is to describe the chewing neural control and oral bolus qualication. A review the cranial

nerves involved with swallowing and their relationship with the brainstem, cerebellum, base nuclei and cortex was made. Methods – From the reviewed

literature including personal researches and new observations, a consistent and necessary revision of concepts was made, not rarely conicting. Re-

sults and Conclusion – Five different possibilities of the swallowing oral phase are described: nutritional voluntary, primary cortical, semiautomatic,

subsequent gulps, and spontaneous. In relation to the neural control of the swallowing pharyngeal phase, the stimulus that triggers the pharyngeal

phase is not the pharyngeal contact produced by the bolus passage, but the pharyngeal pressure distension, with or without contents. In nutritional

swallowing, food and pressure are transferred, but in the primary cortical oral phase, only pressure is transferred, and the pharyngeal response is

similar. The pharyngeal phase incorporates, as its functional part, the oral phase dynamics already in course. The pharyngeal phase starts by action

of the pharyngeal plexus, composed of the glossopharyngeal (IX), vagus (X) and accessory (XI) nerves, with involvement of the trigeminal (V), facial

(VII), glossopharyngeal (IX) and the hypoglossal (XII) nerves. The cervical plexus (C1, C2) and the hypoglossal nerve on each side form the ansa

cervicalis, from where a pathway of cervical origin goes to the geniohyoid muscle, which acts in the elevation of the hyoid-laryngeal complex. We also

appraise the neural control of the swallowing esophageal phase. Besides other hypotheses, we consider that it is possible that the longitudinal and

circular muscular layers of the esophagus display, respectively, long-pitch and short-pitch spiral bers. This morphology, associated with the concept

of energy preservation, allows us to admit that the contraction of the longitudinal layer, by having a long-pitch spiral arrangement, would be able

to widen the esophagus, diminishing the resistance to the ow, probably also by opening of the gastroesophageal transition. In this way, the circular

layer, with its short-pitch spiral bers, would propel the food downwards by sequential contraction.

HEADINGS – Deglutition. Cranial nerves. Brain stem. Basal ganglia. Cerebral cortex. Neural pathways.

Declared conflict of interest of all authors: none

Disclosure of funding: no funding received

Universidade Federal do Rio de Janeiro (UFRJ), Centro de Ciências da Saúde, Instituto de Ciências Biomédicas, RJ, Brasil.

Corresponding author: Milton Costa. Orcid: 0000-0003-0245-6020. E-mail: [email protected]

AG-2018-48

dx.doi.org/10.1590/S0004-2803.201800000-45

INTRODUCTION

To understand how the nervous system controls any biological

process, we must know what are the necessary afferent and efferent

impulses, where they came from, what is their destination and which

functions integrate this process

(1)

. Swallowing is a motor process

with a very difcult neurophysiological study, and subject of several

discordances

(2)

. These observations and the literature review show

that great part of the accepted mechanisms for the neural control

of swallowing could not be considered trustworthy hypotheses. In

this way, the neural control of swallowing remains as a research

eld, open to new considerations.

The swallowing process is formed by the oral, pharyngeal

and esophageal phases

(2,3)

, with much controversy involving their

mechanisms. Great evolution has been obtained with observations

of neurological lesions and many are the methods available for

conrmation of the hypotheses that, in the end, remain as just

hypotheses. Nevertheless, there is an expressive quantity of new

morphological and functional conceptions that, even being only

hypotheses, at least are more structured than the empirical others

used until now to explain the swallowing mechanisms.

It had been believed that the swallowing control center was

located exclusively in the brainstem, and that the entire swallowing

mechanism, automatic and semiautomatic movements of chewing

and swallowing, were involuntary by genesis and regulation. From

observations of patients with cortical dysphagia, the role of the

cerebral cortex in the swallowing control mechanism has been

recognized and extensively studied

(4)

Based on the nervous system embryology a rhombencephalic

center, formed by association of the third primitive vesicle (hind-

brain) with the second one (mesencephalon or midbrain), origin of

the brainstem and cerebellum was described. The rhombencephalic

center would receive stimuli produced by the food bolus passage over

existing receptors at the base of the tongue, on the palatoglossal

and palatopharyngeal pillars, on the palate, and pharyngeal walls,

especially in the posterior one, starting an involuntary and coor-

dinated process that would characterize the pharyngeal phase of

swallowing. The assumption was that this phase would be controlled,

in physiological circumstances, by a framework continuously modi-

ed by peripheral afferent stimuli that would especially inuence the

muscular function, adjusting strength and time of contraction to

the size of bolus swallowed. The bolus entrance in the oropharynx

would produce soft palate elevation and reex contraction of the

upper pharynx constrictor. In addition, to protect the airways, the

bolus entrance would initiate a peristaltic wave that would propagate

to the other muscles, narrowing the pharynx, except at the level of

the cricopharyngeal muscle, which would relax, allowing the passage

of the pharyngeal content to the esophagus

(5)

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62 • Arq Gastroenterol • 2018. v. 55. Suplemento

A center involving sensory and motor nuclei integrated by a

network of interneurons located in the brainstem complements the

described coordination

(6,7,8)

A new approach considers the oropharynx functional activity

as composed by the oral and pharyngeal phases of swallowing

(2,9,10)

This functional activity would be produced by muscular contrac-

tion, and coordinated by a control center in the brainstem, desig-

nated as the Central Pattern Generator (CPG) for Swallowing

(9,11-15)

This pattern-generating center would consist of two hemicent-

ers, one on each side of the brainstem, which, under physiological

conditions, would synchronize and organize the bilateral contrac-

tion of the oral and pharyngeal muscles. Their nerve bers would

cross the midline of the brainstem, interconnecting the two halves

of the involved generating centers with swallowing-linked neurons

in the dorsal and ventral regions of the brainstem

(16,17)

It has been admitted that in this pattern-generating center the

solitary tract nucleus would receive information that would con-

verge to it both from peripheral impulses triggered by the swallow-

ing stimulus and from the cerebral cortex

(9,18)

. This convergence of

stimuli to the solitary tract nucleus would be primarily important

for the induction of voluntary swallowing

(15)

. It’s been considered

that the rst event observed in the “swallowing reex” would occur

in the oropharyngeal cavity (oral and pharyngeal cavities), where

the bolus would produce a sensory afferent stimulus that would

inform the brainstem and cortex

(19-21)

In nutritive swallowing, the rst cortical command would be

sent to the solitary tract nucleus. Thus, eating and drinking sequen-

tially could be voluntarily initiated or facilitated by the cerebral

cortex through the neural network (CPG) of the brainstem

(2,20,22,23)

It was also considered that, in voluntary deglutition, regions of

the cortex and subcortical areas related to swallowing would serve

mainly to trigger and control the onset of the swallowing motor

sequence, especially the oral phase

(20)

In disagreement with the bilateral integration of the brainstem,

admitted in the pattern-generating center conception

(9,11-15)

, it has

already been described that both the dorsal (sensory) and ventral

(motor) regions represented on both sides of the brainstem would

be able to independently coordinate the pharyngeal and esophageal

phases of swallowing on each side

(24)

Although the oral and pharyngeal cavities are morphologically

contiguous and have sequential function, the oral and pharyngeal

swallowing phases are distinct from each other in structures, in-

nervation and neural control. The oral phase is voluntary and

the pharyngeal one is reex. Designating the oral and pharyngeal

phases as oropharyngeal or buccopharyngeal

(2,9,10,12,25,26)

is inad-

equate, although not rare. Anatomically, the oropharynx is the

intermediate segment that communicates the oral and pharyngeal

cavities, receiving the contents transferred during swallowing, which

in no way denes the functional role of the oral and pharyngeal

phases of swallowing.

High dysphagia has been often dened as oropharyngeal dys-

phagia. High dysphagia may occur with impairment of both phases,

but the possibility of exclusively oral or pharyngeal injury cannot

be ignored. The fact that the injury of one neighboring phase in-

terferes with the dynamics of the other emphasizes commitment of

the sequence, and not of both phases. The oropharyngeal designa-

tion for this kind of dysphagia diverts the clinical and therapeutic

focuses, which should be directed to the actually compromised

phase, with doubtful therapeutic adequacy. The designation of

oropharyngeal dysphagia led us to misclassify the dysphagia that

affects the oral and pharyngeal phases as transference dysphagia,

and the esophageal dysphagia, as a conduction one. Transference

is proper to the oral phase, and conduction, to the pharyngeal and

esophageal phases. Transference is a voluntary process and occurs in

the voluntary oral phase, and conduction occurs in the pharyngeal

and esophageal phases, both reex

(27)

It is a fact that we have learned very much by observing neu-

rological dysphagia. In addition, today there are many methods

available for study of swallowing and its disorders, which, while

enabling us to better understand the swallowing physiology, high-

light the signicant number of conicting concepts still in force.

The aim of this work is to offer new conceptual alternatives,

based on the literature and personal research, to give a more solid

basis to the hypotheses used to explain the swallowing mechanisms

and, consequently, the neural control of swallowing.

CHEWING

Mastication, basically voluntary, integrates the activation of

the chewing muscles, innervated by the trigeminal pair (V), the

tongue muscles, innervated by the hypoglossal pair (XII), and with

less evident participation, of the expression muscles, in special the

orbicular of the lips and buccinators, which, like other skin-inserted

muscles, are innervated by the facial pair (VII). Trigeminal afferent

bers reach the dorsal region of the brainstem (the main sensory

nucleus of the V) and, still in an afferent pathway through the

trigeminal lemniscus, reach the thalamus, from where axons go to

the postcentral gyrus (somatosensory cortex) in the parietal region

of the cerebral cortex

(1)

. The postcentral gyrus transfers informa-

tion to the precentral gyrus (somatomotor cortex) in the frontal

region, generating a motor efferent response by the nuclear cortical

route (pyramidal-voluntary), which reaches the ventral region of

the brainstem, where on each side the trigeminal motor nucleus is

located. From this nucleus, the motor route of the trigeminal nerve

activates the chewing muscles

(1,28-31)

By activation from the cortex-nuclear pathway, the hypoglos-

sal motor nucleus in the brainstem gives dynamics to the tongue

in its participation in the chewing process. Afferent and efferent

facial nerve pathways, in functional association, participate in the

accommodation of the bolus and in the oral cavity pressure by

adjusting the tension of the cavity walls, especially dependent on

the orbicularis of the lips and buccinators.

The afferent trigeminal bers also reach its mesencephalic

nucleus, which connects its sensory route with its motor root in

absence of cortical relation. This direct, sensory-motor relation-

ship allows the chewing action, which is voluntary, to have a reex

component

(1)

, which, by proprioceptive perception during the

preparation of the bolus, modulates the variation of the chewing

intensity produced by the continuous modication of the resistance

of the bolus under preparation.

ORAL QUALIFICATION

The oral cavity is able to identify several characteristics of the

inner bolus. It presents at least four distinct types of perception,

thermal, painful, mechanical and chemical

(32,33)

The thermal-reception can perceive hot or cold in various

levels. When pleasing and adequate with the type of food, they

can be incorporated to the pleasure of the diet. When extreme and

damaging, they produce rejection.

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Neural control of swallowing

Arq Gastroenterol • 2018. v. 55. Suplemento • 63

The pain-reception is usually due to mechanical, thermal or

chemical hyper-stimuli produced on sensitive afferent pathways,

warning and preventing injury. However, there is a painful sub-

modality produced by capsaicin, present in a large number of

peppers, probably using the same pain way, whose perception is

often perceived as dietary pleasure.

The mechanical-reception allows noticing the contact of the

bolus against the intraoral structures. The tongue that presses the

bolus, gathering information dened as tactile. This information

allows perceiving the physical characteristics of the bolus, detect-

ing if there is impropriety in its contents. Mechanical-reception is

also responsible for the characterization of oral bolus volume and

viscosity, to dene how much motor units must be depolarized for

the necessary generation of oral pressure to transfer the contents

from the oral cavity to the pharynx.

The chemical-reception identies the tastes by different mecha-

nisms. Sweet appears to be identied by coupling of a primary mes-

senger (taste protein) with a secondary messenger (cAMP – cyclic

adenosine monophosphate), whose concentration increase closes

the potassium channels in the gustatory receptors, with membrane

depolarization. It is considered that the intracellular metabolic

pathways responsible for natural sweeteners would be distinct from

those activated by articial sweeteners, whose secondary messenger

would be the IP3 (inositol triphosphate), which would act on the

calcium channels, provoking calcium input into the cells, with depo-

larization. The identication of the bitter taste is given by coupling

of the same primary messenger (taste protein), resulting in calcium

increase due to action of the IP3 secondary messenger, releasing

a neurotransmitter without membrane depolarization. The salty

perception is generated by direct passage of sodium through the

membrane channels that depolarize. The hydrogen from sour or

acid penetrates the cellular membrane by blocking the potassium

channels, which supports the membrane depolarization

(32,33)

Although sweet, salty, sour and bitter are the tastes considered

basic, others like metallic, astringent and more recently, umami

(monosodium glutamate) have been suggested as primary. Nev-

ertheless, the rst four were the ones that resisted as basic over

time. It is not very clear whether and how the association of basic

tastes (sweet, salty, sour and bitter) can appropriately produce the

palate, i.e. the gustatory perception as a whole. The palate, which

can distinct for each of us, is an association of the social level and

learning, basic tastes, tactile and thermal perceptions, and certainly

the impressions permitted by the vision and smell senses

(33,34)

The perception of tastes in the oral cavity has been prioritized

on the tongue. Classic description points to sequential areas on each

side of the anterior 2/3 of the tongue as having selective capacity for

the basic tastes, the anterior tip to sweet, the sides, in sequence to

salty and sour, and the posterior central area, to bitter

(31,34-39)

. This

concept, already contested, shows that the tongue is able to perceive

all the basic tastes in all its regions, with expressive predominance

of the bitter one

(40-42)

The tongue’s liform, fungiform, foliate and circumvallate

papillae are anatomical elements involved with the chemical senses

(taste). These papillae display incrusted gustatory buttons. In the

liform papillae, gustatory buttons are rare or absent. In the fungi-

form ones there are few, but in the foliate papillae and especially in

circumvallate ones, there are many gustatory buttons

(41,42)

Buttons considered as gustatory can be identied, in addition

to the tongue papillae, on the palate and vallecula. Buttons with

similar morphology to those dened as gustatory have been found

on the pharynx regions, where, at rst, no taste is perceived. In

the vallecula, even with the oral cavity anesthetized, the bitter

taste transferred to the pharynx can be perceived by vagus nerve

conduction

(41)

As far as we know, in the oral cavity there have not been de-

scribed or observed any other morphological kind of receptors than

that admitted as gustatory. However, the oral cavity holds several

other perceptions. Specic receptors to be stimulated are supposedly

necessary. Nevertheless, there is no evidence indicating that any

receptor is responsible for detecting only one type of stimulus

(43)

It is possible that receptors deemed gustative are also able

to receive other oral stimuli. This hypothesis is reinforced by the

presence of receptors morphologically similar to the gustatory

receptor, where tastes are not perceived as palate, in the pharynx

(except the in vallecula) and larynx

(34)

. There are also gustatory

perception descriptions by thermal stimulation of the tongue

(44)

such as sweet perception by heating the anterior edge of the tongue

from a cool state, and evocation of acid or salty perception with

cooling intensication

(45)

CRANIAL NERVES

The cranial nerves associated with the swallowing process are

the trigeminal (V),

facial (VII), glossopharyngeal (IX), vagus (X),

accessory (XI) – usually not considered – and hypoglossal (XII).

It should be emphasized that the structures involved in the swal-

lowing process are pairs, both anatomically and/or functionally,

due to the dual-side innervation. Anatomically unique, the tongue,

palate, pharynx and larynx are functional pairs, each side having

independent innervation

(1,7,29,30)

From receptors on each side of the oral cavity, the trigeminal

(V), facial (VII) and glossopharyngeal (IX) nerves conduct in-

formation to the brainstem. These mixed nerves lead sensitivity

(afferent pathway) and motor command (efferent pathway). The

afferent pathways of the anterior two thirds of the tongue are sup-

plied by the lingual nerve, which associates the trigeminal (general

sensibility) with the facial nerve (taste). In the posterior third of

the tongue, both the general sensibility and taste are conducted by

the glossopharyngeal nerve

(33,39,41-46)

In its afferent pathways toward the brainstem, the trigeminal,

facial and glossopharyngeal nerves of both sides will make gan-

glionar synapses similar to the posterior roots of the spinal cord.

The afferent pathway of the trigeminal nerve makes synapses in

the trigeminal ganglion (Gasser), the facial nerve, in the geniculate

ganglion, and the glossopharyngeal, in the rostral ganglion (upper

one)

(1,30,39)

The trigeminal nerve (V) has three branches; upper (ophthal-

mic), middle (maxillary) and lower (mandibular). The upper and

medium are exclusively sensitive, and the inferior, mixed. The sen-

sitive bers of the three branches innervate the face in transverse

bands of representation. Regarding the oral cavity, the middle

branch (maxillary) has sensitive responsibility for the upper arcade

teeth, upper lip, cheeks, hard palate (mouth mucosa) and mucosa

of the rhinopharynx. The sensitive portion of the lower branch

(mandibular) is responsible for the sensitivity of the lower arcade

teeth and lower mucosa of the mouth, as well as by the general

sensitivity of the anterior 2/3 of the tongue

(1,29,30)

From the trigeminal ganglion to the brainstem, all the sensory

pathways will end in the posterior portion of the brainstem, over

the trigeminal sensitive nucleus that occupies the medulla oblongata

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64 • Arq Gastroenterol • 2018. v. 55. Suplemento

(spinal tract nucleus of the cranial nerve V), the pons (main sensory

nucleus of the cranial nerve V) and the midbrain (midbrain nucleus

of the cranial nerve V). Centrally the sensitive bers divide into

short, ascending branches that end in the main sensorial nucleus,

to attend to tactile sensibility, and into long, descending branches

that serve to tact, temperature and pain, also providing collateral

pathways to the spinal nucleus of the cranial nerve V

(29)

It is believed that proprioceptive fibers from the midbrain

nucleus of the trigeminal neve, in synapse with its motor nucleus

located in the upper portion of the pons

(47)

, would be able to inte-

grate important chewing reex arcs

(1,29)

. Unless expressly desired,

these arcs allow reex modulation of chewing intensity based on

bolus consistency variations, even during the voluntary bolus

chewing preparation.

The motor root of the trigeminal nerve emerges from the ventral

portion of the pons and runs through the mandibular root to in-

nervate the chewing muscles, the mylohyoid, the anterior belly of

the digastric and the tensor muscle of the palate

(1,29,30)

The facial nerve (VII) is a mixed one, considering its motor

root in association with the sensitive root given by the intermedi-

ate (Wrisberg) nerve

(1)

. The taste of the anterior two thirds of the

tongue on each side are its responsibility. From the tongue, this

afferent, pre-ganglionic route follows through the lingual nerve

(association of nerves V and VII), and afterwards through the

tympanic cord nerve (facial branch), to make synapses on the

geniculate ganglion. Through the intermediate nerve, the postgan-

glionic bers (afferent visceral special – gustative route) synapse in

the solitary tract nucleus of the medulla oblongata, associated with

the general afferent visceral bers, providing sensitive innervation

to the mucosa of the nasal cavities and soft palate

(1)

The parasympathetic efferent bers of the facial nerve, origi-

nating from the upper salivary nucleus located on each side of

the upper portion of the medulla oblongata, run through the

intermediate nerve and afterwards through the tympanic cord

nerve to make synapses in the submandibular ganglion. Thence,

through postganglionic bers, they stimulate salivary secretion of

the submandibular and sublingual glands

(1)

The motor portion of the facial nerve has its nucleus on the

ventral portion of the pons. Its bers stimulate the skin-inserted

muscles in the face, neck and scalp, as well as the posterior belly

of digastric and stylohyoid muscles

(1,8,29,39)

The glossopharyngeal (IX) nerve comes out of the skull to-

gether with the vagus (X) and accessory (XI) nerves. The visceral

general afferent and the visceral special afferent bers of the glos-

sopharyngeal nerve are associated. The visceral general afferent

bers are responsible for the general sensitivity of the oropharynx

mucosa and the posterior third of the tongue, and the special vis-

ceral afferent bers, for the taste of the posterior third of the tongue.

These preganglionic bers make synapses with the upper ganglion.

The postganglionic bers will end at the solitary tract nucleus

(1,8,29)

The glossopharyngeal nerve’s efferent pathways come from

two distinct nuclei of the medulla oblongata, the salivary inferior

(parasympathetic) nucleus and ambiguous motor (special visceral

efferent) nucleus. The parasympathetic bers stimulate the sali-

vary secretion after synapses with the optic ganglion, from which

postganglionic bers emerge to innervate the parotid gland

(1,29,31)

The glossopharyngeal nerve’s only motor role is with the stylo-

pharyngeus muscle. Nevertheless, it has already been considered as

motor to the superior pharyngeal constrictor muscle, whose activity

had been previously attributed to the vagus nerve, responsible for

the motor innervation of all pharyngeal constrictors muscles

(1,29)

The vagus (X) nerve has relationships extending from the cervi-

cal region to the abdomen (transverse colon). Its sensory afference

(sensory pathway) connects with the solitary tract nucleus located

in the medulla oblongata. The visceral special efference (motor

pathway) comes from the ambiguous nucleus in the ventral region

of the medulla oblongata, and the parasympathetic bers (visceral

general efference), from the dorsal motor nucleus of the vagus

(1,29-31)

The visceral special afferent (taste) and visceral general affer-

ent (sensibility) pathways of the vagus nerve, after synapses in a

peripheral ganglion (lower or caudal), have their postganglionic

bers end at the solitary tract nucleus, similar to that observed in the

intermediate portion of the facial nerve and in the glossopharyngeal

one. The visceral general afferent bers conduct impulses related to

the sensitivity of the pharynx, larynx, trachea and esophagus, and

the visceral special afferent route lead taste stimuli from receptors

on the vallecula and from a small posterior area of the tongue next

to the vallecula

(1)

The visceral general efferent (parasympathetic) bers of the

vagus nerve originate in the vagus dorsal motor nucleus, and from

it, on each side, they gather in a single-trunk, descending pathway,

emitting branches in the cervical, thoracic and abdominal region,

where they end. These preganglionic bers will establish synapses

in peripheral ganglia of the parasympathetic vegetative or autono-

mous nervous system, close to, or even inside, the viscera walls

(1,29-31)

The visceral special efferent (motor) bers of the vagus originate

in the ambiguous nucleus, and are responsible for innervation of

the striated muscles of the pharynx, larynx and esophagus

(1)

The accessory (XI) nerve, not always considered among those

related to swallowing control, presents special visceral efferent

fibers coming from the ambiguous nucleus (motor to striated

muscles of branchial origin) that would join this type of special

visceral efferent bers of the vagus. Thus, in addition to the vagus

(X) nerve, the accessory (XI) one would also be responsible for the

motor innervation of the striated portions of the pharynx, larynx

and esophagus. A possible second association between the vagus

and accessory nerves would be the presence of parasympathetic

bers (general visceral efferent) in the accessory nerve, with origin

in the dorsal nucleus of the vagus, which would accompany the

vagus nerve bers

(1,29,47)

The Hypoglossal (XII) nerve, a motor one, has an individual-

ized nucleus on the ventral-medial portion on each side of the

medulla oblongata. It is responsible for the tongue extrinsic and

intrinsic muscles. In addition, bers from the cervical plexus in

association with the hypoglossal nerve form the ansa cervicalis,

from which a branch from the cervical plexus, usually C1, will

innervate the geniohyoid muscle, one of the responsible for the

hyoid-laryngeal displacement

(1,8,29)

The pharyngeal plexus (glossopharyngeal, vagus and accessory

though vagus) is considered responsible for the pharyngeal reex

phase, where afferent information from the pharynx reach the

brainstem, generating efferent stimuli to the pharyngeal structures

involved in this phase of the swallowing process.

The pressure transfer from the oral cavity to the pharynx by

distention would produce afferent stimuli that would reach the

brainstem, in special the sensitive (solitary tract) nucleus. From the

sensitive nucleus, through interneurons of the reticular formation,

the ventral motor (ambiguous) nucleus of the brainstem gener-

ates efferent motor stimuli to the pharyngeal structures. Several

structural movements initiated during the voluntary oral phase,

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Arq Gastroenterol • 2018. v. 55. Suplemento • 65

remain in progress until the end of the pharyngeal phase, such as

hyoid-laryngeal elevation, swallowing apnea and tongue posterior

projection, to pharynx, started during the oral ejection, without

considering the palate tension produced by the trigeminal nerve.

In this way, several elements of the oral phase incorporated by

the pharyngeal reex phase allow us to consider the pharyngeal

phase as dependent on the cranial nerves V, VII, IX, X, XI and

XII of both sides.

BRAINSTEM, CEREBELLUM, BASE NUCLEI AND CORTEX

The brainstem is formed by the medulla oblongata, the pons

and the midbrain. It contains the cranial nerves’ nuclei related to

swallowing. The sensory nuclei are posteriorly located on both sides,

and the motor ones, anteriorly. Interneurons and pathways of the

reticular formation interconnect the sensory and motor nuclei in

the brainstem. These are also connected with peripheral receptors,

cerebellum, and sensory and motor areas of the cerebral cortex

through base nuclei, and with peripheral effectors like muscles and

salivary glands

(1,8,28-30,39)

The brainstem receives and emits pathways with stimuli infor-

mation to be integrated and distributed. From peripheral receptors,

the brainstem sensitive nuclei will receive peripheral sensitivity

information by general afferent pathways (V, VII, IX), and taste,

by special afferent ones (VII, IX, X). During the oral phase, all

the bolus characteristics are identied and analyzed by the cortex,

which informs the brainstem the pattern to be employed by the

oral effectors. The brainstem, through the motor hypoglossal

(XII) nerve, will stimulate intrinsic and extrinsic tongue muscles.

The other swallowing muscles, as well as those involved in the

pharyngeal phase, will be stimulated by motor bers of visceral

special efferent nerves (V, VII, IX, X and XI). The brainstem also

depolarizes visceral general efferent parasympathetic pathways

to salivary glands (nerves VII and IX)

(8,29,30)

. The vagus (X), and

maybe the accessory (XI), send preganglionic parasympathetic

bers to the autonomic digestive system, through bers from the

vagus dorsal nucleus

(1,29,47)

In the brainstem, swallowing cranial nerves’ pathways make

functional connections with the cerebellum. The swallowing cra-

nial nerves go in and out of the cerebellum through the inferior,

middle and superior cerebellar peduncles. The inferior one receives

mainly afferent signals, the medium, only afferent signals, and the

superior, mostly efferent signals. Specic longitudinal pathways

interconnect brainstem and cerebellum nuclei with base nuclei and

cerebral cortex. In this way, the cerebellum and cerebral cortex can

interfere with the mechanics to be effected by the cranial nerves’

pathways in the swallowing process

(1,8,29)

In addition to balance and muscle tone, the cerebellum acts by

determining the temporal sequence of the synergistic contraction

of the different skeletal striated muscles, which can generate delay

of the motor signals by fractions of a second. It also acts by se-

quencing the motor activities from one movement to another, and

can control the relation of agonist and antagonist muscles. When

necessary, the cerebellum also can make adjustments in the motor

activities produced by other parts of the brain

(1,8,29)

Ascending and descending cerebellar pathways connect the

cortex and the cerebellum. Originated in large parts of the premotor

and motor cortex, the so-called cortex-pons-cerebellar pathway fol-

lows to nuclei in the pons and thence to the contralateral hemisphere

of the cerebellum. The signs that enter the cerebellum connect with

its nuclei and go out to send signals that are distributed to other

parts of the brain. The cerebellar pathway, whose role is to help

coordinate the motor activity sequences initiated by the cerebral

cortex, originates in the cerebellar cortex and, after connection with

one of its main nuclei (dentate), goes to the thalamus and will end

in the cerebral cortex

(8)

. Swallowing has its motor control bilaterally

represented in the cerebral cortex

(48-51)

. This bilateral representation

means that peripheral stimuli reach both cerebral hemispheres,

with admitted dominance of one of them. This dominance as-

sumes that, in physiological conditions, the dominant hemisphere

inhibits the function of the contralateral one. In dysphagia due to

involvement of the dominant hemisphere, it has been observed that

the contralateral hemisphere can increase its representation, with

apparent functional recovery

(52-54)

The oral phase, being voluntary, allows us to decide whether

to swallow the oral content. The cortical area with the oral control

capacity has been identied in the lower portion of the precentral

gyrus (frontal cortex) and postcentral gyrus (parietal cortex), where

sensitivity (somatosensory cortex) and motor control (somatomo-

tor cortex) are separated by the central sulcus

(55,56)

. (FIGURE 1).

The intraoral qualication, linked to sensory pathways of the

cranial pairs V, VII and IX, with nuclei in the brainstem, will have

visceral afferent general and special stimuli conducted thought base

nuclei up to the cerebral cortex. From the cortex, efferent direct

or indirect commands (involving the base nuclei) reach the motor

nuclei of the brainstem, under cerebellar mediation, from where

the motor pathways of these nerve pairs coordinate the dynamics

of the peripheral effectors

(1,8,29,30)

Afferent pathways of nerves V, VII and IX go to the cerebral

cortex. From the trigeminal (V) sensory nucleus, tactile sensitivity

pathways pass to the thalamus and cortex trough secondary dorsal

tracts. From the spinal nucleus of the cranial pair V, tactile, pain and

temperature pathways go to thalamus and cortex via the secondary

ventral tract. The facial (VII) and glossopharyngeal (IX) nerves

connect with the cerebral cortex through sensitive bers coming

from the solitary tract nucleus through medial lemniscus and

FIGURE 1. Lateral view of an anatomical specimen (brain), highlighting

the sensory, postcentral and the motor, precentral gyrus, separated by

the central sulcus. The main anatomical elements are described over

the gure. 1, 2 and 3: areas of somatosensory cortex; 5 and 7: sensitive

association areas; 4: motor cortex; and 6: premotor area.

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66 • Arq Gastroenterol • 2018. v. 55. Suplemento

thalamus. The efferent pathways from the cortex to the brainstem

motor nuclei of these three pairs of cranial nerves, modulated by

the cerebellum, occur with bilateral (mainly cross) connections of

the cortex-nuclear tract (voluntary). These voluntary pathways will

end in the brainstem in connection with the motor nucleus of the

nerves V and VII, as well as with motor neurons of the pair IX in

the ambiguous nucleus

(28,29)

ORAL PHASE OF SWALLOWING

The oral phase can be classied into ve subtypes: 1) Nutrition-

al voluntary oral phase; 2) Primary cortical voluntary oral phase;

3) Semi-automatic oral phase; 4) Subsequent gulps oral phase;

and 5) Spontaneous oral phase. These ve oral phase possibilities

occur in association with pharyngeal and esophageal reex phases.

Nutritional voluntary oral phase

The nutritive swallowing following chewing, with the bolus

prepared and qualied, will put it usually over the tongue (organize)

and transfer it (eject) to the pharynx

(57)

. The voluntary oral phase of

swallowing leads information to the cortex by the afferent pathways

of the nerves V, VII and IX (mixed pairs) that allow the cortex to

activate the motor portions of these mixed nerves in association

with the hypoglossal (XII – motor pair). Originating in peripheral

receptors, afferent pathways reach the brainstem. From the sensory

nuclei of the cranial pair V, through the secondary ventral and

dorsal tracts, they reach the thalamus and cortex with tactile (also

volume and viscosity), thermal and possibly nociceptive sensations.

Afferent general (sensitivity) and special (taste) pathways led by the

cranial nerves VII and IX reach the solitary tract nucleus in the dor-

sal region of the medulla oblongata. From this, afferent pathways

connect with the base nuclei, including thalamus, and then with

the cerebral cortex on the postcentral gyrus of both hemispheres,

transferring the received afferent signals to the precentral gyrus,

from where efferent pathways go to the brainstem motors nuclei

(V, VII, IX, XII).

Based on the hemisphere dominance, one can conclude that

both afferent general (sensitive) and special (taste), and efferent

special (motors) and general (parasympathetic) pathways intercon-

necting both sides of cortex and brainstem arrive and leave as direct

and cross paths. This organization gives to each cerebral hemisphere

the total information collected in the oral cavity, enabling effective

commands from each hemisphere to reach both sides of the brain-

stem, integrating the cranial nerves that act in the oral phase

(58)

After activating the sensorial cortex on both sides from the base

nuclei, the peripheral information passes to the motor cortex, where

the necessary intensity is modulated and re-transmitted to the base

nuclei and brainstem. In the latter, the efferent pathways of the

trigeminal, facial and hypoglossal nerves would produce an oral

dynamic that would end by ejecting its contents into the pharynx.

Although one of the hemispheres is dominant, both are fully

informed, allowing them to exercise full functions

(48-51)

. There is

evidence that the dysphagia generated by injury to the dominant

hemisphere allows increase in the representation of the non-dom-

inant (non-injured) hemisphere, associated with apparent function

recovery

(52-54)

. There are pathways crossing from one side to the

other through the corpus callosum, integrating the hemispheres.

Thus, in healthy individuals, the dominant cortex can exert inhibi-

tory action on the contralateral one by a connection that passes

through the corpus callosum. It is also possible to consider the

existence of excitatory pathways from the dominant motor cortex

to the base nuclei of the contralateral hemisphere. This organization

would explain not only the already evidenced function recovery

when there is lesion of the dominant hemisphere

(52-54)

, but also the

integrated bilateral stimulus that is observed, despite the inhibition

of the sensorial and motor cortex of the non-dominant hemisphere.

It is also possible to assume that these excitatory pathways exist

in both directions.

Between the brainstem and the cortex, there are also intercon-

nected pathways arriving at, and leaving from, the cerebellum,

considered able to modulate muscular contraction intensity and

sequence. In this way, cerebellar pathways connect with efferent vol-

untary (cortex-nuclear) pathways that will make synapses with the

motor nuclei of the cranial nerves V, VII, IX and XII. From these

nuclei, the efferent stimuli follow to the oral effectors, providing

them with signaling of adequate contraction intensity and sequence,

coordinated by the cortex and modulated by the cerebellum.

The bolus volume and viscosity will interfere with the muscular

contraction intensity, dened by the cortex according to the oral

qualication, to generate the necessary oral ejection. Nevertheless,

the contraction activation sequence of the effectors will be common

to all sequences involving the oral phase, suggesting that the neural

organization has a predened sequence. Taste and temperature

do not exert inuence on the oral muscular contraction intensity

dened by the cortex. This observation means that, within limits of

acceptability, chemical-reception, thermo-reception and certainly

pain-reception do not interfere with the oral activity, which is

governed by the mechanical reception, in particular volume and

viscosity, which will affect the amount of motor units to be depolar-

ized for an effective oral phase. The generation of the necessary and

adequate muscular contraction intensity will be responsible for the

information to be passed and maintained during the reex phase

of swallowing. The pressure intensity transferred by the oral phase

will be the stimulus to be answered to by the neural control of the

reex pharyngeal phase. The esophageal phase, also reex, should

be inuenced at least partly by the oral phase

(57,58)

One can describe the basic dynamics of the swallowing oral

phase as follows: The Dental arcades touch one another by chewing

muscle contraction (pair V). This dental arcades position allows

skin-inserted muscles, in special buccinators and orbicularis oris

(pair VII), to generate intraoral pressure resistance to prevent

pressure escape out of the oral cavity during the bolus transfer-

ence to the pharynx. The pressurized and resistant oral cavity

will enable ejection of the bolus by the tongue (pair XII), which

will transfer pressure and bolus to the pharynx. Still as part of

the oral phase actions, the tensor veli palatini muscle (pair V) will

provide resistance to the soft palate, which will be superiorly and

posteriorly projected by the levator veli palatini muscle against the

rst fascicle of the pharynx superior constrictor muscle (pterygo-

pharyngeus fascicle) at the beginning of the pharyngeal phase.

The suprahyoid muscles elevate the hyoid and larynx, opening the

pharyngeal-esophageal transition because it undoes the tweezers

action between the vertebral body and larynx. The elevation of

the hyoid and larynx that acts by undoing of the tweezers action,

produced by the apposition of the larynx against the spine is co-

ordinated mainly by the cranial nerves V and VII and also by C1

through the ansa cervicalis. The hyoid elevation starts at the end

of the oral phase, and stays active till the end of pharyngeal phase.

Contraction of the longitudinal stylopharyngeus muscle (IX) will

reduce the pharyngeal distal resistance. Finally, in the end of oral

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Neural control of swallowing

Arq Gastroenterol • 2018. v. 55. Suplemento • 67

phase, by possible involvement of the respiratory center on the

oor of the fourth ventricle in the brainstem, swallowing apnea

(preventive apnea) takes place. In sequence, but with an independent

mechanism of apnea, beginning the pharyngeal phase, vocal folds

adduction will occur. All the oral events remain active during the

entire pharyngeal phase by assimilation of the reex pharyngeal

phase coordination

(42,59-63)

. (FIGURE 2).

this type of neural control does not have, as an integral part, the

afferent signaling coming from the oral receptors to the sensitive

cortex. In this way, the sequence from the motor cortex to the oral

effectors will be exactly the same

(58)

Semiautomatic oral phase

This type of neural control is a temporary substitute for the one

that occurs during the nutritional swallowing process. It replaces the

voluntary control of the nutritional oral phase when, in a repetitive

way, this has its parameters qualied and accepted as usual and

within appropriate limits. In such cases, if the attention has been

divided with another interest that demands cortical activity, swal-

lowing control can be replaced by a semiautomatic control, which

will be processed in subcortical level (base nuclei). Considering the

proposed organization for the integration between base nuclei and

cortex, we can hold that the base nuclei take control of the oral

phase, maintaining its integrative activity, but repressing in their

level the information brought from the periphery. Nevertheless,

the base nuclei retain the ability to reactivate cortical control at

any time, in particular if changes are detected

(58)

. I believe that the

dominant hemisphere controls this semiautomatic process from

its base nuclei, also through corpus callosum, on the same way of

the inhibitory control.

Subsequent gulps oral phase

Subsequent gulps oral phase swallowing in subsequent gulps

implies liquid intake that, in healthy individuals, demands depo-

larization of fewer motor units, because the necessary ejection force

does not require too much effort. The control of this oral phase type

of swallowing is, at least for the rst gulp, similar to the control of

nutritional swallowing. Although the material to ingest is liquid, a

proper qualication is necessary, since it may have characteristics

unexpected or distinct from the appearance. Taste, temperature

and viscosity are assessed during the rst gulp and, if accepted,

go promptly to semiautomatic coordination, similar to that occur-

ring in the nutritional diet. Here, the semiautomatic dynamics can

start without requesting any other cortical attention, and without

losing the basic perception of the gulps’ characteristics. Like in

nutritional swallowing, the resumption of the voluntary cortical

control is immediate if desired or if any irregularity is perceived.

Spontaneous oral phase

Spontaneous oral phase is the swallowing that occurs to clarify

oral cavity of the saliva produced and released in discrete volumes,

but continuously. This type of oral phase occurs repeatedly over the

course of the day’s 24 hours, with the individual awake or asleep, in

the absence of conscious control. These swallowing efforts generate

a mechanical sequence similar to the other swallowing types with

origin in the oral cavity. However, in some respect it is distinct in

its trigger mechanisms. I believe that is possible to assume that this

type of swallowing is due to the airways protective mechanism to

prevent aspirations and compromising of the respiratory system.

It has been demonstrated that the saliva adsorbed to the mucous

membrane is capable of lubricating the laryngeal vestibule and

vocal folds without producing discomfort. Also, the resulting

volume of accumulated saliva would be compressed between the

vestibular folds and epiglottis tubercle during swallowing with the

adduced vocal folds, resulting in return of the residual saliva to the

pharynx

(64)

. It is possible to believe that spontaneous swallowing is

a product of this physiological airways permeation.

FIGURE 2. Frontal view of schematic diagram over an anatomical

specimen representing the neural control of the nutritional oral phase.

Black, dotted lines represent the oral afferent pathways that pass through

the (1) sensorial ganglion and connect with sensitive nuclei of the solitary

tract and nerve V nuclei in the brainstem (2). From there, they connect

with the base nuclei (3) through direct and cross pathways. From the base

nuclei (3), in nutritious swallowing the signals stimulate the postcentral

(sensorial) and precentral (motor) gyruses (4), which start the efferent

(motor) pathway. (Note 1: Sensory pathways do not exist in the primary

cortical voluntary oral phase). Red, solid lines represent efferent motor

pathways from the cortex to the base nuclei (3) and brainstem nuclei (2)

where nerves V, VII, IX and XII conduct the stimuli (modulated by the

cerebellum) to the oral effectors. (Note 2: In semiautomatic swallowing

and while normality is maintained, motor responses are produced

without cortical intervention). From the dominant hemisphere, there

is an inhibiting pathway (black, dashed line) going to the opposite

hemisphere and an excitatory pathway (red, solid line) and also to the

base dominant nuclei to the non-dominant side.

Primary cortical voluntary oral phase

This type of oral phase reproduces all dynamic events ob-

served in the nutritive oral phase of swallowing, without having

any intraoral content to be qualied. It happens as if the cerebral

cortex imagined a bolus with such known features, that the effer-

ent cortical motor area reproduces an oral ejection with the same

characteristics and using the same efferent pathways that it would

if that imagined bolus could be exposed to oral receptors. Thus,

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68 • Arq Gastroenterol • 2018. v. 55. Suplemento

The spontaneous swallowing that occurs repeatedly, being the

individual awake or during sleep and in the absence of conscious

control, seems to be the same semiautomatic swallowing observed

in the nutritious swallowing sequence, though with a distinct trigger

mechanism, probably related to airway protection.

Besides other functions, saliva is important in the chewing bolus

preparation and in the lubrication of the mucous membranes to

suitable transport. Saliva is produced in continuous volume and

physical-chemical characteristics by the salivary glands, with me-

diation of parasympathetic bers conducted by the cranial nerves

VII (facial) and IX (glossopharyngeal).

Spontaneous swallowing helps in the distribution of saliva over

the oral, pharyngeal and even vestibular mucosa, humidifying these

membranes and probably helping to maintain uid the mucus over

the laryngeal ventricles. Inhalation and expiration dry the mucosa

by the continuous airow, and spontaneous swallowing keeps the

moisture level of these mucous membranes. Spontaneous swal-

lowing is also important for the control of small volume of liquids

adsorbed to the laryngeal vestibule walls, removing any excess over

this mucosa. During swallowing, with the adduced vestibule folds,

the tubercle of the epiglottis presses against these folds, making

the vestibule lumen virtual, expelling to the pharynx any excess

existing there

(58,64)

NEURAL CONTROL OF THE

SWALLOWING PHARYNGEAL PHASE

The reex pharyngeal phase takes place without voluntary

control or direct cortical command. This phase starts from the phar-

yngeal pressure stimulus transferred by the oral phase. In nutritional

swallowing, after bolus qualication, in special in relation to volume

and viscosity (mechanoreceptors), the oral ejection will transfer the

qualied information (bolus and pressure) to the pharynx. From

there the perceived stimulus go to the brainstem (solitary tract

nucleus). In the brainstem, in special in the ambiguous nucleus, a

motor reex response will determine sequential muscle contractions

in delay line based on the values qualied and transferred by the

oral phase

(58,65,66)

. Delay line is the contractile sequential muscular

response of the muscles involved in the pharyngeal phase to a

single pressure stimulus, which departs from the pharynx to the

posterior sensory portion of the brainstem, and which returns to

it via a ventral motor pathway, producing the sequential dynam-

ics of the pharynx contractile activity. Although there is no direct

motor cortex inuence on the pharyngeal phase, the transferred

content can be perceived, for example, for its temperature. This

kind of perception means that there is afferent sensitivity, possibly

to provide the oral transfer with tolerance limits.

The stimulus that triggers the pharyngeal phase is not the

contact produced by the passage of food through the pharynx

(67,68)

but the pressure that distends it, with or without contents

(58,69)

. In

nutritional swallowing, food and pressure are transferred, but in

cortical swallowing, only pressure is, and the pharyngeal response

is similar to that of nutritious swallowing, indicating that the pres-

sure distending the pharyngeal walls is the element that stimulates

the pharyngeal motor activity

(58)

The pharyngeal distention pressure is identied and transferred

to the brainstem through sensitive afferent bers of the pharyn-

geal plexus (cranial nerves IX, X, XI). The glossopharyngeal (IX)

nerves in the oropharynx and vagus and accessory (X and XI) in

the laryngopharynx carry to the brainstem dorsal region (solitary

tract nucleus – sensitive) the stimulus based on the pressure value

transferred from the oral cavity to the pharynx. The dorsal region

(sensitive) and the ventral one (motor) are integrated by interneu-

rons of the brainstem’s reticular system. A unique stimulus reaches

the solitary tract nucleus, and motor reex response is composed by

a sequential action of several muscles in different times, conguring

muscular sequential contraction in delay line.

It is reasonable to admit a cerebellum modulation over the

pharyngeal reex responses determined by the brainstem, explain-

ing the sequential muscular contraction in the pharyngeal phase

(delay line). Among its main functions, the cerebellum coordinates

the temporal sequence of the synergic contraction of the different

skeletal striated muscles, with the possibility to generate delay of

the motor signals by fractions of a second, creating delay in the

muscle contraction sequence

(1,8,29)

In a didactic way, and not failing to admit the possibility of a

delay line control by inhibitory neurotransmitters, we have consid-

ered that the sensory-motor connection in the brainstem would be

carried out by distinct amounts of synapses between interneurons

connecting sensitive and motor nuclei, generating different transfer

times between the solitary tract nucleus to the ambiguous one. Thus,

a stimulus perceived by the pharyngeal receptors and transmitted to

the solitary tract nucleus as unique would be retransmitted to the

ambiguous nucleus, passing by a different and increasing number

of interneurons, conguring the delay line observed in the swal-

lowing pharyngeal phase.

Besides the sequence and intensity of muscular contraction

determined by the brainstem from pressure reception, the phar-

yngeal phase incorporates or assimilates, as its functional part,

the oral phase developments already in course. The oral phase

incorporated elements and the pharyngeal phase will end together.

Therefore, the brainstem, during the pharyngeal phase, integrates

the sequence of the oral phase with the pharyngeal one. The phar-

yngeal phase starts by action of the pharyngeal plexus, composed

of the glossopharyngeal (IX), vagus (X) and accessory (XI) nerves,

with secondary involvement of the trigeminal (V), facial (VII),

glossopharyngeal (IX) and the hypoglossal (XII), and also some

elements of the cervical plexus (C1, C2). The cervical plexus and

the hypoglossal nerve on each side form the ansa cervicalis, from

which a pathway goes to the geniohyoid muscle, one of the muscles

that act in the elevation of the hyoid-laryngeal complex

(58,65,70,71)

The accessory (XI) nerve, not always considered among those

associated with swallowing, is admitted as having special visceral

efferent (motor) bers originating from the ambiguous nucleus

that would follow associated with the vagus nerve, which would

also display this type of ber

(1,47)

. Thus, the accessory (XI) nerve

is also responsible for the motor innervation of the musculature

of the palate, pharynx, larynx and esophagus, in association with

the vagus nerve.

The pharyngeal phase shows adjustment, over the tongue on

each side, of the palatoglossal muscle, innervated by the motor

portion of the pharyngeal plexus (X, XI) to prevent pressure from

returning to the oral cavity. The tension (V) and elevation of the

palate (X, XI) against the rst fascicle (pterygo-pharyngeal) of

the upper constrictor muscle of the pharynx, innervated by the

cranial nerves X and XI, blocks the possible pressure escape from

the oropharynx to the rhinopharynx.

The superior, middle and inferior constrictor muscles of the

pharynx are each one constituted of distinct parts, with individu-

alized insertions. Each one of these parts is inserted in one side

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Neural control of swallowing

Arq Gastroenterol • 2018. v. 55. Suplemento • 69

in anterolateral xed points, and in the other, in the posterior

median line of the pharynx (pharyngeal raphe). As a consequence

of the individualization of their motor units, they can contract in

sequential mode. The superior constrictor muscle has four parts

(pterygopharyngeal, buccopharyngeal, mylopharyngeal and glos-

sopharyngeal), the middle, two parts (chondropharyngeal and

ceratopharyngeal), and the inferior, two parts (thyreopharyngeal

and cricopharyngeal). The cricopharyngeal presents two fascicles,

the upper, oblique, and the lower, transverse, whose bers seems to

cross with each other’s in the midline. Between the two fascicles of

the cricopharyngeal muscle, there is an anatomically less resistant

area due muscular absence

(72)

The four parts of the superior constrictor occupy the entire

extension of the oropharynx. Thus, it is necessary that only the

rst portion of its superior (pterygopharyngeal) part perform

apposition against the palate, isolating and preventing pressure

escapes from the oropharynx to the rhinopharynx. In the same

time, the oral pressure can pass to the pharynx without resistance.

The sequential contraction of the superior, middle and inferior

constrictors’ parts do not generate pharyngeal peristalsis, since

there is no circular muscle on the pharyngeal wall. With closing

of the pharyngeal contiguous cavities except for the pharyngeal-

esophageal transition, which opens as a result of the elevation of

the hyoid and larynx, there is a constrictors muscle contraction

generating a pressure sequence in the cranial-caudal direction. This

pressure sequence displaces the transient bolus from the pharynx

to the permissive, less resistant esophagus by the opening of the

pharyngeal-esophageal transition

(42,70)

By denition, peristalsis is a sequential expression produced by

a muscle circular layer. In this way this cranial-caudal pressure se-

quence with distal less resistance without muscle circular layer should

not be considered as peristalsis or peristalsis like as is often dened.

The suprahyoid muscles are innervated by the cranial nerves V

and VII and by the (C1) cervical plexus, connected via ansa cervica-

lis with the hypoglossal nerve. The mylohyoid branch of mandibular

nerve (mixed root of trigeminal – V) innervates the mylohyoid and

the anterior belly of the digastric muscles; the posterior belly of the

digastric and the stylohyoid muscles, by the facial nerve (VII). The

geniohyoid and thyrohyoid muscles are innervated by ansa cervica-

lis (usually C1) through the hypoglossal (XII) nerve. The cervical

plexus (usually C2) through the ansa cervicalis innervate the other

infrahyoid muscles. The suprahyoid muscle group is responsible

for the forward and upward movement of hyoid and larynx, with

modulation by the infrahyoid group. This action moves the larynx

away from the vertebral body and opens the pharyngeal-esophageal

transition. Moreover, while moving the larynx away, the suprahyoid

group is able to sustain this open condition depending on the bolus

volume and viscosity. The opening of the pharyngeal-esophageal

transition is also enhanced by the contraction of the longitudinal

pharyngeal muscles, the stylopharyngeal ones, innervated by the

glossopharyngeal (IX) nerve, and the palatopharyngeal muscle,

innervated by motor bers from cranial nerves X and XI

(42,65,71,72)

Still in the oral phase, as a last act, a preventive apnea (swal-

lowing apnea) ensues, being assimilated by the pharyngeal phase

and remaining until its end. Associated with the airways resistance

produced by apnea, there is independent vocal folds adduction (X,

XI), followed by closure of the vestibular folds with the bolus pas-

sage through the already open pharyngeal-esophageal transition.

The adduction of the vestibular folds is due to the compression of

the pre-epiglottic fatty cushion produced by the elevation of the

hyoid and larynx, which compresses this cushion contained in the

pre-epiglottic brous space. This space has, as its point of least

resistance, the lateral aspects of the tapered end of the epiglottis,

which corresponds to the projection of the vestibular folds on both

sides. Thus, the compression produced by this fatty cushion on

the sides of the epiglottis causes the medial shift of the vestibular

folds, which end up in apposition against the epiglottis tubercle.

On its turn, the epiglottis, everted by the tongue, moves posteriorly,

adjusting its tubercle against the now adduced vestibular folds

(59-62)

At the same time, the constrictor muscles’ parts, including the

crycopharingeal one, carry out the sequential, cranio-caudal con-

traction (nerves X and XI), driving the bolus from the pharynx

into the esophagus

(62,63)

. (FIGURE 3).

FIGURE 3. Neural control representation of the pharyngeal phase over

anatomical specimens where 1 – oral cavity, 2 – pharynx, 3 – esophagus,

4 – swallowed bolus, 5 – brainstem, X – pharyngeal receptors, 6 –

solitary tract nucleus, 7 – Ambiguous nucleus. Over 5, lower dotted

arrows from six to six – afferent integration, and upper dotted arrows

from six to seven – efferent integration. From 6 (sensitive nucleus) to 7

(motor nucleus), multi-dotted arrows are a didactic representation of the

growing number of interneurons of the delay line. From 7 (ambiguous

nucleus) to a, b, and c on both sides, dashed arrows represent the efferent

stimulus to muscle delay line. There is pressure transference from 1

to 2 (pharyngeal distention), represented by widening of 4. Hollow

arrowheads show displacement of the bolus (4) from mouth to esophagus.

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70 • Arq Gastroenterol • 2018. v. 55. Suplemento

The pharyngeal and esophageal phases, both reex, present

anatomical and functional relation. The rsts 10 cm of the es-

ophagus are formed by skeletal striated muscle, like the oral and

pharyngeal ones. In the distal extremity of this striated segment,

by 2 or 3 cm, a muscular distinction is identied macroscopically in

fresh anatomical specimens, which is microscopically dened as a

mixture of skeletal striated muscle (long and multinucleated bers)

and bers of smooth muscle (short and mono-nucleated), where

the rst ganglion of the myenteric plexus appears

(73)

. (FIGURE 4).

The cricopharyngeal muscle has been known as a skeletal

striated muscle type that demands expressive consumption of

ATP (adenosine triphosphate), because it depends on ATP both

to contract and to relax. In order to demonstrate that the cri-

copharyngeal muscle is not contracted at rest, only to relax when

the pharyngeal-esophageal transition opens, as believed by many,

we performed manometry of the pharyngeal-esophageal transi-

tion. This manometry was carried out with a balloon built with

a latex glove nger to measure the positive pressure resistance of

the pharyngeal-esophageal transition of 12 fresh corpses, in the

rst 6 to 12 hours postmortem. This research were permitted by

an agreement between the Anatomy Department of the Biomedi-

cal Sciences Institute of the Federal University of Rio de Janeiro

(Universidade Federal do Rio de Janeiro – UFRJ) and the Legal

Medical Institute of Rio de Janeiro, Brazil.

The balloon traction shows that positive pressure values remain

present on the pharyngeal-esophageal transition in all studied fresh

corpses. A second pressure verication, with insertion of a metal-

lic prosthesis between the vertebral body and the larynx, shows

absence of resistance in this region, where the prosthesis eliminates

the tweezer mechanism of the larynx against the vertebral body.

Based on the positive values observed in the rst measure and

absent in the second, with the prosthesis insertion, we concluded

that resistance on the pharyngeal-esophageal transition is depend-

ent on the tweezer action of the larynx against the vertebral body.

(FIGURE 6).

In two cricopharyngeal muscles, we also carried out electric

stimulation, including analysis of tolerance to calcium pump

inhibitors (verapamil) and polyacrylamide gel electrophoresis

with dodecyl sodium sulfate paired with other striated muscles.

FIGURE 4. A – fresh esophagus segment where there is mixture of 1

– smooth and 2 – striated muscle. B – histological specimen obtained

from (A), with (1) rst ganglion of the myenteric plexus and mixture of

long and multinucleated striated muscle bers (2) and short and mono-

nucleated smooth ones (3).

The high-pressure zone designated as the upper esophageal

sphincter is located at the distal pharynx, where a tweezer action

closes the pharynx between the larynx (cricoid cartilage) and the

cervical lordosis at the level of the 5th to 6th cervical vertebrae.

Usually this high pressure is considered as due to the maintained

contraction of the cricopharyngeal muscle, part of the inferior

pharyngeal constrictor. This conception is a severe misunder-

standing about the anatomical and functional characteristics of

this region. The inferior constrictor of the pharynx is a skeletal

striated muscle consisting of two fascicles (thyropharyngeal and

the cricopharyngeal). The cricopharyngeal fascicle presents two

parts of bers in its organization, an upper, oblique and a lower,

transverse. The upper one inserts on each side of the cricoid car-

tilage, from where its bers go from the bottom upwards and from

lateral to medial, inserting on the posterior pharyngeal raphe. The

lower or transverse part inserts on each side of the cricoid cartilage,

with a transverse direction, intercrossing in the midline, where the

raphe cannot be seen. The width of the pharyngeal lumen at the

level of the transverse cricopharyngeal part is about 17 mm and

there is not muscular ring in this region, which can be described

as a muscular half-curvature. The divergence between the oblique

and transverse parts of the cricopharyngeal muscle creates an

intermediary zone without muscular bers that constitutes an

anatomically less resistant point, already described as the Kilian

zone, where the posterior pharyngeal diverticulum, known as

Zenker’s diverticulum, can occur. This anatomically less resistant

area is coincidentally the point of higher-pressure values, certainly

due to the tweezer action produced by the vertebral body and the

larynx

(65,71)

. (FIGURE 5).

FIGURE 5. Posterior view of anatomical specimen involving the

pharynx, larynx, esophagus and trachea, where 1 – Cricopharyngeal

muscle, oblique fascicle, 2 – Cricopharyngeal muscle, transverse fascicle,

inserted on the larynx cricoid cartilage, 3 – Kilian zone, the anatomically

less resistant zone on the posterior pharyngeal wall where the pharyngeal

diverticulum described by Zenker occurs. This less resistant zone

is due to the divergence of the oblique and transverse fascicles of the

cricopharyngeal muscle. 4 – Trachea, 5 – Esophagus.

Costa MMB.

Neural control of swallowing

Arq Gastroenterol • 2018. v. 55. Suplemento • 71

We obtained these two cricopharyngeal muscles from specimens

immediately resected from total laryngectomies, with surgical indi-

cation and consent. These muscles showed the same characteristics

of other striated muscles under electric stimulation, including their

tolerance to calcium pump inhibitors. The electrophoresis paired

with other striated muscles revealed the same protein patterns and

molecular weights. These two experiments allow the conclusion

that the cricopharyngeal muscle has morphology and function of

a striated muscle. (FIGURES 7 and 8).

The open pharyngeal-esophageal transition intercommunicates

the pharynx and esophagus, allowing the video-uoroscopic exami-

nation to show the ow of contrast medium lling both cavities

almost simultaneously. One can observe that the pharyngeal and

esophageal cavities present a relation with the contrast medium that

occurs during the time of the pharyngeal phase. Thus, the beginning

of the esophageal phase occurs, practically, in the same time of the

pharyngeal phase, demonstrating the clear functional relationship

between these reex phases, which is so much or more consistent

than the observed between the oral and pharyngeal phases. This

fact demonstrates that the pharyngeal and esophageal phases are

responsible for the conduction of the contents transferred by the

oral phase

(61,74)

. (FIGURE 9).

NEURAL CONTROL OF THE

SWALLOWING ESOPHAGEAL PHASE

The sequential contraction of pharyngeal muscles leads the

bolus transferred by pharyngeal pressure. It results from the special

visceral efferent innervation conducted by the vagus nerve, origi-

nating in the ambiguous nucleus, also responsible for the striated

muscle of the upper portion of the esophagus. The bolus inside

the esophagus is conducted by sequential contractions in distal

direction, dened as primary peristalsis.

The mechanical relation between bolus and smooth muscle in

the esophagus wall will be able to stimulate this kind of muscle,

unlike striated one. The smooth muscle in the esophagus wall will

FIGURE 6.A. Manometry on a fresh corpse. B. Scheme highlighting (a) – pharynx between tweezer formed by vertebral body and larynx that compresses

the pharynx at rest, (b) – elastic and distensible balloon, and (c) – sphygmomanometer. (d) – rectangle containing three possibilities of pressurization of

the system, where X represents ow closure, 1 and 2 represent air ow to be balanced with the distended balloon, and 3, the three-way tube that allows the

balance of pressures, (e) – syringe, 4 – direction of balloon traction. C. After verication of basal pressure (positive in all 12 cases), cervical dissection for

passage of a metallic prosthesis separating the larynx from the spine. D. Prosthesis installed for re-verication (absence of positive pressure in all 12 cases).

FIGURE 7. Polygraphic record of isometric tension of the

cricopharyngeal muscle. On top, the polygraph used. The rst bar shows

constant increase of the contraction force as the stimuli intensity (Volts)

increases. The second bar shows gradual contraction frequency increase

of the cricopharingeal muscle with the stimuli pace (Hz) increment,

until the installation of tetany. The third bar shows the use of verapamil

(calcium pump blocker) in increasing concentrations: both in the

absence and with increasing doses of the calcium pump blocker, the

muscle behavior is the expected for skeletal striated muscle. The three

bars therefore register a skeletal striated muscle behavior.

Costa MMB.

Neural control of swallowing

72 • Arq Gastroenterol • 2018. v. 55. Suplemento

FIGURE 8. Protein Electrophoresis. On the right side, protein fractions distribution near the same plane for the four tested muscle samples, where two

are cricopharyngeal samples and two other muscles previous known as striated (extensor halluces longus and soleus muscle). On the left, superposition

of the protein weights of the four tested muscle samples, conrming that the cricopharyngeal muscles has the similar protein fractions distribution of

the previous known as striated muscle.

FIGURE 9. Video-uoroscopic examination of swallowed contrast media. 1 – Oropharynx, 2 – Epiglottis, 3 – Piriform recesses, 4 – Pharyngeal-

esophageal transition, and 5 – Esophagus. The pharyngeal phase begins at frame 20 and ends at 50, with total time of 0.99 sec. (each frame lasts

0.033 msec.). After 0.2 to 0.23 sec. (frame 26 to 27), the esophageal phase is already starting in superposition with the pharyngeal one. The epiglottis

remains in the vertical position and will only close the pharyngeal-esophageal communication (horizontal position) at the end of the pharyngeal phase,

in frame 45. At this time, the pharynx, with residual volume, starts its return to resting position, with closure of the pharyngeal-esophageal transition

by the return of the larynx in opposition to the vertebral body and with the epiglottis in vertical position.

Costa MMB.

Neural control of swallowing

Arq Gastroenterol • 2018. v. 55. Suplemento • 73

capable of interfering with the tonus and motility of the smooth

portion of the esophagus

(1)

. It is also believed that the esophagus

distal extremity presents resting tonic contraction involving the

distal circular musculature. Hormones would regulate this resting

tonic contraction in association with intrinsic and extrinsic nerves

that generate pressure values around 20 mmHg. This prevailing

hypothesis considers that the gastroesophageal transition opens

to due muscle relaxation that would occur in association with the

primary peristalsis, induced by vagus bers that would inhibit the

tonic contraction of the circular musculature, with possible media-

tion of VIP (vasoactive intestinal polypeptide) neurotransmitters

and NO (nitric oxide)

(77)

Despite the prevailing concepts, it has not been identied, in the

distal portion of the esophagus, a muscular ring with the classical

characteristics observed in smooth muscle sphincters. However, the

gastroesophageal transition, without muscular thickening, presents

positive resting pressure, which fades away during the primary

peristaltic wave that leads the bolus to the stomach. Due to the

lack of knowledge about the morphology responsible for the high

pressure of this transition dened as cardia, it has been deemed a

physiological sphincter. This situation has given rise to speculations

that add up to about 27 possible mechanisms, isolated or in associa-

tion, including those involving the regional muscle organization

(74)

The esophagus presents an internal layer, dened as circular,

and another external, as longitudinal. The external one, when

contracting, reduces the resistance of the esophageal tube, and

the internal propels the bolus in sequential contraction. It is pos-

sible that the esophageal muscular layers are arranged in a way

that the external layer displays long-pitch, spiral bers, and the

internal one, short-pitch, spiral bers. This morphology, associated

with the concept of energy preservation, allows us to admit that

the contraction of the external layer would be able to widen the

esophagus, decreasing the resistance to the ow, probably also by

opening the gastroesophageal transition. On its turn, the internal

layer would propel the food downwards by sequential contraction.

Thus, during the resting esophageal stage, there would be no energy

expenditure

(58,73,74)

. The opening of the gastroesophageal transi-

tion would be an active response to the esophageal peristalsis that

would activate the myenteric plexus during the entry of the bolus

into the esophagus. Corroborates this hypothesis the fact that the

esophagus, when subjected to pure pressure distension, responds

differently than in the presence of the concrete bolus.

be depolarized in a syncytial way, where the depolarization of the

muscle cells is freely transferred from one to the other, with con-

traction processed in the entire extension of the muscle layer. Thus,

we can consider, as a hypothetical mechanism, that the contents

transferred from the pharynx to the esophagus while in its striated

portion are conducted similarly to the way that takes place in the

pharynx, by depolarization of motor units. Nevertheless, when the

bolus passes through the striated/smooth transition, it is capable of

stimulating the myenteric plexus from this transition on, generating

syncytial contraction. This syncytial depolarization is able to cause

contraction of the longitudinal layer, reducing the resistance of the

esophagus as a whole, increasing its complacency and culminating,

or at least participating, in the opening of the gastroesophageal

transition that occurs in concomitance with the onset of primary

peristalsis. It is also possible that the circular musculature depolar-

izes and contracts during the bolus passage through the striated/

smooth transition, in association with the primary peristalsis. This

contraction pressurizes the esophageal lumen downwards, leading

the bolus in transit through the esophagus

(75-76)

The pharynx and the esophagus rst portion are both formed

by striate muscle innervated by the special visceral efferent (motor)

pathway of the vagus nerve. This cranial nerve also has the general

visceral efferent (parasympathetic) pathway, which is preganglionic

to the myenteric plexus. In this way, another hypothesis would be

that the esophageal smooth muscle motor coordination be done by

myenteric postganglionic stimulation in sequence with the special

visceral efferent pathway (motor to striate muscle) in association

with the general visceral efferent pathway (parasympathetic - motor

to smooth muscle) of the vagus nerve.

The contents transferred from the pharynx to the esophagus,

notably the ones with solid fragments, not always reach the stomach.

Sometimes they stop at the level of the esophagus smooth muscle,

from where they are able to locally stimulate the submucosal plexus,

which transfers an activation command to the myenteric plexus, pro-

ducing muscle contraction from the retention point on. This down-

ward contractile wave is dened as secondary peristalsis, which ends

up conducting the residual esophageal contents to the stomach

(73)

It has been considered that the general visceral efferent path-

way (parasympathetic bers) originating in the posterior motor

nucleus of vagus as preganglionic bers will connect to intrapa-

rietal ganglia in the esophageal wall, from where postganglionic

bers connect with visceral effectors that release neuro-hormones

Costa MMB.

Neural control of swallowing

74 • Arq Gastroenterol • 2018. v. 55. Suplemento

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Costa MMB. Controle neural da deglutição. Arq Gastroenterol.

RESUMO – Contexto – A deglutição é um processo motor com muitas discordâncias e de difícil estudo quanto a sua neurosiologia. Talvez por essa razão

sejam tão raros os artigos sobre esse tema. Objetivo – Descrever o controle neural da mastigação e a qualicação do bolo que se obtém durante a fase

oral. Revisar os nervos cranianos envolvidos com a deglutição e suas relações com o tronco cerebral, cerebelo, núcleos de base e córtex. Métodos – Re-

visão da literatura com inclusão de trabalhos pessoais e novas observações buscando dar consistência a necessária revisão dos conceitos, muitas vezes

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oral nutricional voluntária, fase oral cortical voluntária primaria, fase oral semiautomática, fase oral em goles subsequentes e fase oral espontânea.

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