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Erschienen in: Insights into Imaging 4/2018

Open Access 13.06.2018 | Pictorial Review

Tracking the glossopharyngeal nerve pathway through anatomical references in cross-sectional imaging techniques: a pictorial review

verfasst von: José María García Santos, Sandra Sánchez Jiménez, Marta Tovar Pérez, Matilde Moreno Cascales, Javier Lailhacar Marty, Miguel A. Fernández-Villacañas Marín

Erschienen in: Insights into Imaging | Ausgabe 4/2018

Abstract

The glossopharyngeal nerve (GPN) is a rarely considered cranial nerve in imaging interpretation, mainly because clinical signs may remain unnoticed, but also due to its complex anatomy and inconspicuousness in conventional cross-sectional imaging. In this pictorial review, we aim to conduct a comprehensive review of the GPN anatomy from its origin in the central nervous system to peripheral target organs. Because the nerve cannot be visualised with conventional imaging examinations for most of its course, we will focus on the most relevant anatomical references along the entire GPN pathway, which will be divided into the brain stem, cisternal, cranial base (to which we will add the parasympathetic pathway leaving the main trunk of the GPN at the cranial base) and cervical segments. For that purpose, we will take advantage of cadaveric slices and dissections, our own developed drawings and schemes, and computed tomography (CT) and magnetic resonance imaging (MRI) cross-sectional images from our hospital’s radiological information system and picture and archiving communication system.

Teaching Points

The glossopharyngeal nerve is one of the most hidden cranial nerves.
It conveys sensory, visceral, taste, parasympathetic and motor information.
Radiologists’ knowledge must go beyond the limitations of conventional imaging techniques.
The nerve’s pathway involves the brain stem, cisternal, skull base and cervical segments.
Systematising anatomical references will help with nerve pathway tracking.
Hinweise

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Introduction

The glossopharyngeal nerve (GPN) or IX cranial nerve is one of the most unattended cranial nerves in imaging examinations. It is not depicted for most of its course and, when affected, clinical manifestations are usually not characteristic. In fact, the GPN and vagus nerve interact so closely that an isolated GPN dysfunction might not be clinically discriminated if vagus nerve function is not impaired [1], except in the particular case of glossopharyngeal neuralgia [15]. When a cranial nerve injury is suspected, the nerve’s pathway must be considered from the brain stem to the target organs [3]. In a conventional magnetic resonance imaging (MRI), the vast majority of cranial nerves are generally visible only in a short segment but are affected by visible diseases. Therefore, by deepening anatomic knowledge, radiologists who interpret cross-sectional images can partially overcome that limitation.
Previous radiological publications have not been especially focused on the anatomic relationships of cranial nerves or on the GPN. Those reviews have placed more emphasis on diseases that may affect the cranial nerves [3, 4, 68]. For that reason, and based on an electronic poster (EPOS) presented at the 2013 European Congress of Radiology [9], the aim of this article is to review the GPN from an anatomical point of view, based on schematics, illustrations and cadaveric specimens, and to identify the anatomical references that indicate the path of the nerve in cross-sectional images. The involvement of the GPN’s pathway in pathological processes is beyond the scope of this anatomical review, and the reader can find other imaging reports elsewhere [3, 4, 68].

Functional anatomy and clinical manifestations

The GPN conveys: (1) sensory afferents (retroauricular region), visceral afferents (posterior third of the tongue, pharyngeal tonsil, posterior pharynx, middle ear and Eustachian tube) and taste afferents (posterior third of the tongue); (2) parasympathetic afferents (carotid sinus baroreceptors and carotid body chemoreceptors) and efferents (parotid gland); and (3) motor efferents (stylopharyngeus muscle) [1, 2, 816]. It plays a role in swallowing, which involves a reflex arc that begins at the taste buds located in the posterior third of the tongue and stimulates the parotid to secrete an ideal amount of saliva fluid for swallowing [1, 16]. It also carries somatosensory information from muscles and the ear, the pharynx and tongue mucous, and information from the carotid sinus [1, 2, 816]. Therefore, though isolated involvement is rare, clinical manifestations of a GPN injury may be external earache, mild dysphagia and taste changes in the posterior third of the tongue; the swallowing reflex will be altered on the side of the lesion, the uvula will be deviated to the contralateral side and the sensitivity of the pharynx, palate and tongue will be affected. Changes in the quantity and quality of saliva may be present due to parotid involvement, and tachycardia carotid sinus dysfunction could be affected; finally, glossopharyngeal neuralgia, similar to trigeminal neuralgia, is an isolated GPN process that occurs very occasionally and is characterised by lancinating pain at the base of the tongue and palate [14].

Imaging studies

The images retrieved and included in this manuscript were acquired in a multislice spiral computed tomography (CT), GE LightSpeed VCT 64 (Milwaukee, WI, USA) and a GE Signa HDx 1.5T MRI scanner (Milwaukee, WI, USA). All images corresponded to clinical examinations performed according to our standard cranial, skull base and cervical CT and MRI protocols (Table 1).
Table 1
Clinical computed tomography (CT) and magnetic resonance imaging (MRI) protocols used in the current review
CT protocol
Acquisition
Detector coverage
Pitch
Table speed
Rotation time
Kv
mA max
ASIR
Matrix
FOV
Skull base
Spiral
20 cm
0.531:1
10.62 cm/s
1 s
120
600
40%
512
25 cm
Cranial
Spiral
20 cm
0.531:1
10.62 cm/s
0.8 s
120
280
40%
512
25 cm
Neck
Spiral
20 cm
0.531:1
10.62 cm/s
0.8 s
120
280
40%
512
25 cm
MRI protocol
Sequence
TR
TE
TI
ET
BW
Matrix
FOV
ST
SP
NEX
Brain
T2W axial
5600 ms
100 ms
22
41.67 KHz
512 × 384
26 cm
5 mm
1 mm
2
T2W coronal
4400 ms
102 ms
22
50 KHz
256 × 256
24 cm
5 mm
1 mm
2
T2W coronal
2800 ms
102 ms
22
41.67 KHz
320 × 256
24 cm
3 mm
0 mm
2
Cervical
T1W sagittal
3000 ms
22 ms
Auto
9
41.67 MHz
384 × 224
26 cm
3 mm
0 mm
2
Neck
T1W axial
475 ms
10 ms
3
20.83 KHz
256 × 256
18 cm
4 mm
1 mm
2
T2W axial
4200 ms
85 ms
13
15.63 MHz
256 × 256
18 cm
4 mm
1 mm
3
T1W coronal
350 ms
7 ms
3
31.25 MHz
256 × 192
18 cm
4 mm
1 mm
1
Kv kilovoltage; mA max maximum milliamperage; ASIR adaptive statistical iterative reconstruction; FOV field of view; TR time of repetition; TE time of echo; TI time of inversion; ET echo train; BW bandwidth; ST slice thickness; SP spacing; NEX number of excitations

Cross-sectional anatomy

For the purpose of systematisation, we will follow the pattern of Policeni and Smoker [3]. According to these authors, the path of the lower cranial nerves is divided into the brain stem, cisternal, cranial base (to which we will add the parasympathetic pathway leaving the main trunk of the GPN at the cranial base) and cervical segments, which, in this case, is practically reduced to the suprahyoid compartment [4].

Origin in the brain stem

The GPN and vagus nerve are mixed nerves that contain motor, branchial, sensory and autonomic fibres [16]. Both nerves have a common origin in the upper medulla oblongata and share three nuclei: the motor, the parasympathetic and the special sensory nuclei. Moreover, they convey general sensory information into the spinal trigeminal tract [13, 8, 11, 1517]. Briefly, the motor nucleus involves the upper end of the nucleus ambiguous and innervates the stylopharyngeus muscle. The lower salivary nucleus sends efferent fibres to the parotid gland. General cutaneous and visceral sensory information travels through the GPN, joins the spinal trigeminal tract and ends in the spinal trigeminal nucleus. Finally, the special sensory nucleus is the solitary tract or gustatory nucleus. It receives taste sensation fibres through the solitary tract. The nucleus of the solitary tract also receives afferent impulses from the carotid sinus through the GPN [13, 7, 8, 10, 13, 1517]. All nuclei are located behind the inferior olivary nucleus (Fig. 1).

Brain stem exit and cisternal segment

The GPN emerges in the cerebellomedullary cistern from the medulla oblongata immediately below the bulbopontine sulcus at the level of the retro-olive groove, between the inferior olivary nucleus and the inferior cerebellar peduncle [7, 8, 10] (Fig. 1). At this level, it is immediately above the vagus and spinal nerves (Fig. 2). Within the cistern, the three nerves rest on the posterior margin of the jugular tubercle of the occipital bone (Figs. 2 and 3), crossing laterally close to the anterior and inferior margin of the flocculus and the choroid plexus protruding from the fourth ventricle (Fig. 3). When it arrives at the skull base, the GPN enters an exclusive cranial exit near the top of the jugular foramen [10, 13, 14] (Fig. 2). The cranial nerves are visible in the cistern with MRI [4, 15, 18, 19] but not with CT, so the cerebellar flocculus, the choroid plexus and the jugular tubercle become critical anatomical references.

The jugular foramen and parasympathetic segment

The cochlear aqueduct, opening just above the GPN entrance in the jugular foramen [14, 15, 1921], is the first anatomical reference (Figs. 3 and 4). In the jugular foramen, the GPN runs through the anteromedial portion or pars nervosa (petrosal fossula), separated from the posterolateral portion or pars vascularis (exit for the vagus and spinal nerves and the internal jugular vein) by the jugular spine (Fig. 2) and a fibrous septum (petro-occipital ligament), which is sometimes ossified [3, 6, 8, 13, 14]. At the entrance to the foramen, the GPN, vagus and spinal nerves are initially arranged in an obliquely posteroanterior-lateromedial distribution, between the jugular bulb (posterolateral) and the inferior petrosal sinus (anteromedial) [21] (Fig. 2). Once at the exit of the jugular foramen, the GPN is generally in front of the inferior petrosal sinus before draining into the internal jugular vein [6, 20, 21] (Figs. 2 and 5). Still within the foramen, the GPN shows two focal expansions or nodes [11] (Fig. 1), which are normally not visible in sectional high-resolution clinical images at 1.5T MRI [18] but have been observed with 3T MRI [21]. The superior node conveys general sensitive information and is located next to the opening of the cochlear aqueduct [21]. The lower node (Andersch node) handles the visceral sensory, gustatory and carotid [6, 16] innervations, and is located approximately 3 mm below [21].
The tympanic nerve or Jacobson nerve leaves the GPN from the lower node [1014]. Fibres of the GPN course through this nerve and have a long cranial and parapharyngeal path, jumping from cranial nerve VII (the facial nerve) to cranial nerve V (the trigeminal nerve), and targeting the parotid gland finally. The first anatomical reference for the Jacobson nerve is the inlet of the lower tympanic canaliculus in the jugular spine, which enters just when leaving the GPN [3, 6] and through which it reaches the medial wall of the tympanic cavity at the level of the cochlear promontory [7, 14, 22] (Figs. 2, 4 and 6). Inside the tympanic cavity, the nerve forms a submucosal plexus that conveys sensitive information from the middle ear mucosa, antrum, mastoid air cells and Eustachian tube [3, 8, 10, 1315]. At the level of the tendon of the tensor tympani muscle, it gives off a small nerve branch (deep great petrosal nerve) that will bind the lesser superficial petrosal nerve coming from the geniculate ganglion of the facial nerve [6, 11, 12, 23]. The course of the resultant nerve (the lesser petrosal nerve) can be followed by identifying the geniculate ganglion and the ducts in front, until the nerve enters the middle cranial fossa through the accessory hiatus, lateral to the exit of the greater petrosal nerve, which exits through the fallopian hiatus [1012] (Fig. 6).
Once in the middle cranial fossa, it crosses forward and medially to leave the skull variably through different exits: the foramen spinosum, foramen ovale, innominate canaliculus (located between these two foramen) or the sphenopetrosal junction [11, 23] (Figs. 6 and 7). Immediately below the skull, the GPN fibres synapse in the otic ganglion, medial to the mandibular nerve and just under the foramen ovale [1013] (Fig. 7). The GPN postganglionic fibres leave the otic ganglion through the auriculotemporal branch of the trigeminal nerve. Now, the reference is the line that connects the mandibular nerve with the middle meningeal artery. The auriculotemporal nerve embraces the artery and then goes back through the parapharyngeal space medial to the lateral pterygoid muscle first and the neck of the mandibular condyle later, to reach the deep lobe of the parotid gland, providing it with parasympathetic innervation [8, 10, 11, 14, 22] (Fig. 7).

Cervical segment

Immediately after leaving the jugular foramen, the GPN is located medial to the internal jugular vein and behind the internal carotid artery (Figs. 5 and 8). Now it is located in the retro-styloid or carotid space [4, 24]. When proceeding down the neck, the GPN initially has the same vascular relationships. The styloid process, the most lateral reference at this level, is also a useful mark [10, 12]. At the level of the C1 transverse process, the nerve goes around the carotid artery laterally and descends behind the styloid process and the stylopharyngeus muscle [14] (Fig. 8). When it crosses between the internal carotid artery and the internal jugular vein, the GPN gives off the carotid sinus and carotid body nerve (Hering’s nerve), which descends along the anterior wall of the internal carotid artery [11] (Fig. 9).
Once the GPN is anterior to the vascular structures, it leaves the close relationship with the internal carotid artery approximately at the level of the soft palate [24] and runs behind the styloid muscles (stylohyoid, styloglossus, stylopharyngeus) (Fig. 10). These muscles form a tripod that will be the reference until the nerve enters the oropharynx, especially the medial (stylopharyngeus) and the anterior (styloglossus) muscles. The styloid muscles are surrounded by a fibrous fascia (styloid diaphragm); muscles and fascia form the styloid pyramid [14] (Fig. 9). The GPN surrounds the external side of the stylopharyngeus muscle to reach its anterior surface inside the pyramid [11]. In this course, the GPN provides motor innervation to the muscle [14, 25, 26]. Once within the pyramid, the most common position of the GPN is in a triangle, in which the posterior margin is the external carotid artery, the lower one is the facial artery and the anterior one is the styloglossus muscle [27] (Fig. 9). However, this reference appears not to be suitable for the common axial slices, in which the long axis of the styloid pyramid area might be an easier anatomical key point (Fig. 10).
At approximately the point where the stylopharyngeus muscle merges with the constrictor muscles, the GPN enters the pharynx between the upper and middle constrictors [14]. At this point, the stylopharyngeus and hyoglossus muscles separate the hypoglossal nerve (lateral) from the GPN (medial). This circumstance occurs immediately above the level of the intermediate tendon of the digastric muscle [14] (Fig. 10).
Once in the pharynx, the GPN splits into pharyngeal branches, which contribute to the pharyngeal plexus of the vagus, and the lingual branch [4, 6, 10, 14, 25]. The references of the lingual branch are the lower edge of the palatine tonsil (palatoglossus and styloglossus muscles) and the hyoglossus muscle. The lingual branch reaches the tongue medial to the hyoglossus muscle to innervate the posterior third of the tongue [6, 11] (Fig. 10).
All anatomic references are summarised in Fig. 11.

Glossopharyngeal nerve dysfunction: denervation signs

Muscle denervation can be the most visible sign of neural injury, especially in larger muscles [5, 28, 29]. However, the GPN only innervates the small stylopharyngeus muscle, for which no cases of atrophy have been reported [5, 28]. It also contributes to the pharyngeal plexus of the vagus nerve, which supplies the palatoglossus and palatopharyngeus muscles, the middle and upper constrictors, and the levator muscle of the soft palate [5]. Therefore, secondary changes in cross-sectional images due to GPN denervation cannot be separated from those caused by vagus nerve injuries (Fig. 11). Imaging features are characterised by the soft palate descent at the side of the lesion, a deviated uvula to the opposite side and muscle asymmetries at the level of the torus tubarius and constrictor muscles [1, 26, 28]. Functional parotid gland changes may be unnoticed, as the other salivary glands remain unaffected [1]. More debatable is the possibility of secondary gland atrophy after denervation. Parotid atrophy has been reported in cases of chronic trigeminal denervation, as the auriculotemporal nerve conveys the gland innervations [30]. Though we found no previous articles on parotid gland atrophy related to lesions affecting the GPN pathway, tympanic neurectomies were reported to show that atrophy [31] and the radiologist should consider this possibility (Fig. 12).

Conclusion

The novelty of this article is the specific focus on the glossopharyngeal nerve (GPN) in cross-sectional imaging, which systematises the anatomical relationships of the main trunk and its branches. It will help radiologists obtain insights into a cranial nerve that, unlike many of its counterparts, remains beyond the observer’s attention due to its inconspicuous clinical signs and scarce visibility in normal and pathological clinical images.

Acknowledgements

The manuscript comes from an electronic poster presented as an educational exhibit during the European Congress of Radiology (ECR) held in Vienna in March 2013, where it was distinguished with a cum laude award. The poster is available in the EPOS database through the following link: https://​doi.​org/​10.​1594/​ecr2013/​C-1419.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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Metadaten
Titel
Tracking the glossopharyngeal nerve pathway through anatomical references in cross-sectional imaging techniques: a pictorial review
verfasst von
José María García Santos
Sandra Sánchez Jiménez
Marta Tovar Pérez
Matilde Moreno Cascales
Javier Lailhacar Marty
Miguel A. Fernández-Villacañas Marín
Publikationsdatum
13.06.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Insights into Imaging / Ausgabe 4/2018
Elektronische ISSN: 1869-4101
DOI
https://doi.org/10.1007/s13244-018-0630-5

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