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Annals of Anatomy 195 (2013) 205–211

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Annals of Anatomy
journal homepage: www.elsevier.de/aanat

Education

Anatomical study of the roots of cranial parasympathetic ganglia:


A contribution to medical education
Kvetuse Lovasova a,∗ , Igor J. Sulla b , Adriana Bolekova a , Igor Sulla c , Darina Kluchova a
a
Department of Anatomy, Faculty of Medicine, Pavol Jozef Safarik University in Kosice, Srobarova 2, 041 80 Kosice, Slovak Republic
b
Department of Neurosurgery, Faculty of Medicine, Pavol Jozef Safarik University in Kosice, Tr. SNP 1, 040 66 Kosice and Institute of Neurobiology, Slovak Academy of Sciences,
Soltesovej 4, 040 01 Kosice, Slovak Republic
c
Department of Anatomy, Histology and Physiology, University of Veterinary Medicine and Pharmacy in Kosice, Komenskeho 73, 041 81 Kosice, Slovak Republic

a r t i c l e i n f o s u m m a r y

Article history: A major key to increasing the safety of cranial surgery is a thorough understanding of anatomy. The
Received 1 January 2012 anatomy of the head is of fundamental interest to dental and medical students early in their studies.
Received in revised form 5 January 2013 Clinically, it is mostly relevant to surgeons who are performing interventions and reconstruction in the
Accepted 6 January 2013
maxillofacial region, skull base, and the orbit. However, the level of appropriate anatomical knowledge
Available online 21 February 2013
necessary for general and special medical and surgical practice is still under discussion. This study maps
the significant areas and structures of the head that are not normally accessible during dissection courses
Keywords:
because of time and difficulties involved in the preparation. The detailed photodocumentation enriched
Anatomy
Ciliary ganglion
by diagrams provides a view of structures until now only partially documented. Three parasympathetic
Otic ganglion ganglia are located in hardly accessible areas of the head – inside the orbit, infratemporal fossa, and in
Pterygopalatine ganglion the pterygopalatine fossa. No detailed photographs have been found in current anatomical textbooks and
Roots atlases in relation to the morphology of fibers (roots) connected to the ciliary, otic, and pterygopalatine
Education ganglia. Therefore, this study focused on the detailed display of sensory, sympathetic, and parasympa-
Clinical importance thetic roots of ganglia to provide relevant photodocumentation and an improvement in human anatomy
teaching. This study also confirms that cadaver dissection provides an excellent opportunity for the inte-
gration of anatomy and clinical medicine into the early clinical training of undergraduate dental and
medical students. We believe this article, because of the details mentioned above, will be beneficial not
only for the future anatomical undergraduate but also for postgraduate education.
© 2013 Elsevier GmbH. All rights reserved.

1. Introduction However, some ganglia are difficult to visualize and identify due
to their small size and complicated access. Such is the case of
As the quality, depth, and effectiveness of medical education the three parasympathetic ganglia located in the cranial part of
improves, new methods become available for the teaching of the parasympathetic nervous system (Siéssere et al., 2008). These
anatomy. Anatomical knowledge is fundamentally important to the are: the ciliary, otic, and pterygopalatine ganglia. The fourth,
study and practice of medicine. Despite the availability of a wide parasympathetic submandibular ganglion lies in the region of the
range of high quality anatomical texts and atlases on the current neck, but, as to difficulty of preparation, it belongs to the rela-
medical market, there is no publication with detailed, colorful, illus- tively easily accessible structures, so we did not include it in this
trative photographs of the cranial parasympathetic ganglia that can study.
serve as a visual aid for the teaching of their anatomy to students It is common knowledge that the cranial parasympathetic
of dentistry and general medicine. There is a need for a publication ganglia listed above receive preganglionic fibers through the oculo-
to point out in detail the contribution that an understanding of this motor (CN III), facial (CN VII), and glossopharyngeal (CN IX) nerves.
area of anatomy will make to clinical medicine. Sympathetic and sensory fibers (roots) also enter the ganglia, but
Parasympathetic ganglia of the head are situated inside the do not synapse in them (Kahle and Frotscher, 2002; Lanz and
orbit, infratemporal fossa (ITF), and pterygopalatine fossa (PPF). Wachsmuth, 2004; Siéssere et al., 2008).

1.1. Overview of the anatomy (Fig. 1A–C)


∗ Corresponding author. Tel.: +421 55 234 3209.
E-mail addresses: kvetuse.lovasova@upjs.sk (K. Lovasova),
sullaigorz49@gmail.com (I.J. Sulla), adriana.bolekova@upjs.sk (A. Bolekova),
The ciliary ganglion (Schacher‘s ggl.) is located at the top of the
sulla@uvm.sk (I. Sulla), darina.kluchova@upjs.sk (D. Kluchova). orbit and receives three roots (Fig. 1A):

0940-9602/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.aanat.2013.01.011
206 K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211

Fig. 1. Red – arteries; dark blue – sensory nerves; yellow – sympathetic nerves; light blue – parasympathetic (visceromotor) or somatomotor nerves and ganglion: (A) roots
of the ciliary ganglion and nearby situated structures (lateral view). CN V/1, cranial nerve – 1st division of the trigeminal nerve (ophthalmic nerve); NCN, nasociliary nerve;
CN II, cranial nerve II (optic nerve); CN III, cranial nerve III (oculomotor nerve); LG, lacrimal gland; OA, ophthalmic artery; CG, ciliary ganglion. I., sensory root; II., sympathetic
root; III., parasympathetic root, (B) roots of the otic ganglion and nearby situated structures (lateral view). CN V/3, cranial nerve – 3rd division of trigeminal nerve (mandibular
nerve); ATN, auriculotemporal nerve; CHT, chorda tympani; LN, lingual nerve; IAN, inferior alveolar nerve; MMA, middle meningeal artery; MA, maxillary artery; LPN, lesser
petrosal nerve; OG, otic ganglion; I., sensory root; II., sympathetic root; III., parasympathetic root and (C) roots of the pterygopalatine ganglion and nearby situated structures
(lateral view). CN V/2, cranial nerve – 2nd division of trigeminal nerve (maxillary nerve); GPN, greater petrosal nerve; DPN, deep petrosal nerve; MA, maxillary artery; PPG,
pterygopalatine ganglion; I., sensory root; II., sympathetic root; III., parasympathetic root. (For interpretation of references to color in this figure legend, the reader is referred
to the web version of this article.)

I. The sensory (nasociliary) root enters directly from the I. The sensory root enters the ganglion directly as the ganglionic
nasociliary nerve, through the communicating branch, and does branches of the maxillary nerve (V/3), and does not synapse in
not synapse in the ganglion. the ganglion;
II. The sympathetic root comes from the plexus associated with II. The sympathetic root arises from the plexus associated with
the internal carotid artery and the ophthalmic artery, and does the internal carotid artery. As the deep petrosal nerve (DPN),
not synapse in the ganglion. it enters the ganglion after its emergence from the pterygoid
III. The parasympathetic (oculomotor) root comes from the canal (Vidian canal), and does not synapse in the ganglion.
oculomotor nerve. Preganglionic fibers from the accessory III. The parasympathetic root runs from the facial nerve through the
oculomotor nucleus (Edinger-Westphal ncl.) synapse in the greater petrosal nerve (GPN). It combines with the DPN to form
ganglion (Girijavallabhan and Bhat, 2008; Zhang et al., 2010). the nerve of the pterygoid canal (Vidian nerve), which continues
to the PPF (Rusu et al., 2009; Tubbs et al., 2009).
The otic ganglion (Arnold‘s ggl.) is located at the top of the ITF,
just below the foramen ovale. It receives three roots (Fig. 1B): The location and general morphology of the cranial parasympa-
thetic ganglia in humans have been described in various textbooks
I. The sensory root comes directly from the ganglionic branches and scientific articles (mentioned above), but detailed photographs
of the mandibular nerve (V/3) and does not synapse in the gan- of the roots of the ganglia are lacking in the current anatomical
glion; literature. Our study focused on presenting detailed photodoc-
II. The sympathetic root is derived from the postganglionic fibers umentation of the three parasympathetic ganglia to specifically
of the superior cervical ganglion. Fibers comprising the smallest show their sensory, sympathetic, and parasympathetic roots in
deep petrosal nerve (Tubbs et al., 2009) enter the ganglion from dissected anatomical specimens. This might be very helpful to med-
the plexus of the middle meningeal artery and do not synapse ical students in dissection courses and to all doctors doing surgery
in it; in apposite areas of the head.
III. The parasympathetic root comes from the glossopharyngeal
nerve. Through the tympanic nerve, as the lesser petrosal nerve 2. Materials and methods
(LPN), it arises from the tympanic plexus. The LPN reaches the
ITF and the otic ganglion through either the foramen ovale or This anatomical study was carried out in 10 (20 sides) human
innominate (Arnold‘s) foramen (Tubbs et al., 2005). adult male and female cadaveric heads (3 female, 7 male, age from
50 to 77). The cadaveric material was fixed in 10% formalin and
The pterygopalatine ganglion (Meckel‘s ggl.) lies at the top of the sectioned in a sagittal (median) plane with a manual saw. The heads
PPF, opposite the sphenopalatine foramen. It receives three roots (ganglia) were not specified in terms of gender, age, and side. The
(Fig. 1C): procedures were performed in accordance with the current laws
K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211 207

and written consent of the Scientific Ethic Committee of the Fa- The PPF was revealed after removal of a part of the greater wing
culty of Medicine, Pavol Jozef Safarik University in Kosice, which of sphenoid bone and the zygomatic bone. After removal of the roof
are based on the Helsinki Declaration, 2008. of PPF, the neurovascular structures and the pterygopalatine gan-
A relatively difficult anatomical dissection technique was used glion (PPG) located inside this space were revealed. All roots were
to access the three parasympathetic ganglia. The extended trans- dissected together with additional neuronal (orbital) branches of
cranial, lateral transmandibular, and transsphenoidal approaches the ganglion.
provided wide access to the orbit, infratemporal fossa, and also the The topography of all the examined roots of ganglia was pho-
nearby situated pterygopalatine fossa. Soft and hard tissues were tographically documented with a Canon PowerShot A85 camera
removed using standard methods. (Canon Inc., Tokyo, Japan) and Nikon D80 camera (Nikon Inc., Tokyo,
High resolution photographic techniques are required to Japan).
demonstrate the topography of the neurovascular structures
located in the examined areas. Detailed visualization was achieved 3. Results
by illuminating the ganglia with a point lamp. The ganglia were
exposed from the anterior, anterolateral, lateral, posterolateral, The described dissections inside the skull and at the external
inferolateral, and superior aspects by raising and mobilizing mus- lateral skull base exposed these structures: inside the orbit – the
cles and neurovascular structures. The neurovascular and muscular optic nerve, ophthalmic artery, superior ophthalmic vein, and CG;
relationships of each ganglion were examined. inside the ITF – the mandibular nerve, maxillary artery, and OG;
The orbital area was revealed through the anterior cranial fossa inside the PPF – the maxillary nerve, pterygopalatine portion of
by first removing the cerebral hemispheres and then the orbital maxillary artery, and PPG.
roof. Removal of a part of the lateral orbital wall (greater wing of Muscles and related arterial and nerve branches were also
sphenoid bone and zygomatic bone) afforded a lateral approach as revealed. Periarterial sympathetic plexuses were exposed pre-
well. After removal of the periorbital and retrobulbar fat, the struc- dominantly along the maxillary artery and its locally emerging
tures of the superficial and deep layers were gradually exposed. The branches. The cream-colored cadaveric ganglia and their roots were
extra-ocular muscles were cut and folded away. The ciliary ganglion revealed in all the dissected areas.
(CG) was revealed after pulling away the neurovascular structures
and the lateral rectus. The corresponding roots, as well as structures 3.1. The ciliary ganglion
situated nearby or belonging to the ganglion, were dissected.
The preparative approach to the area of the ITF was carried In 17 cases (85%), the ciliary ganglion appeared as an irregular
out laterally after removal of the soft tissue and exposure of the flattened structure shaped like a star, approximately 2 mm in size,
mandible and zygomatic bone. The otic ganglion (OG) was revealed embedded in the retrobulbar fat near the orbital apex. ln all 20
by folding the main trunk of the mandibular nerve upwards and examined specimens (100%), it was located inferolateral to the optic
backwards after first removing the predominant part of the mas- nerve, between the nerve and the lateral rectus (Figs. 2A and 3A).
ticatory muscles (lateral and medial pterygoid muscles), maxillary The ganglion was covered by the superior ophthalmic vein and the
artery, inferior alveolar nerve, lingual nerve, and auriculotempo- ophthalmic artery (oval field), (Fig. 2A). In 3 cases (15%), we found
ral nerve. The middle meningeal artery and the auriculotemporal that the ganglion appeared as a typical oval body. The long and
nerve were divided for better detailed visualization of all three roots fine sensory root (fibers from the nasociliary nerve; communicat-
of the otic ganglion. ing branch with the ciliary ganglion) passed along the lateral side

Fig. 2. (A) The location of the ciliary ganglion (oval field) inside the orbit and nearby situated neurovascular structures and muscles (superior and anterior view). EB, eyeball;
LRM, lateral rectus; SOV, superior ophthalmic vein; CN II., cranial nerve II (optic nerve); OA, ophthalmic artery; FN, frontal nerve; NCN, nasociliary nerve; SRM, superior
rectus; OT, olfactory tract and (B) A detailed photograph of the sensory root location (superior view). Fine fibers arise from the nasociliary nerve (as communicating branch
with ciliary ganglion) and pass along the lateral side of the optic nerve to reach the upper part of ciliary ganglion. I., sensory root; SRM, superior rectus; SBrIII, superior branch
of oculomotor nerve; LCN, long ciliary nerve; LN, lacrimal nerve; LA, lacrimal artery.
208 K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211

Fig. 3. (A) The location of the ciliary ganglion inferolaterally to the optic nerve (anterolateral view). CN II, cranial nerve II (optic nerve); CG, ciliary ganglion; OA, ophthalmic
artery; SCNn, short ciliary nerves and (B) Roots of the ciliary ganglion (anterolateral view). The sensory and sympathetic roots enter the ganglion posteromedially (sensory
root also from above). The parasympathetic root enters it posterolaterally. Short ciliary nerves arise from the ganglion and run forward in a curving manner above and below
the optic nerve to the area of eyeball posterior pole. I., sensory root; II., sympathetic root; III., parasympathetic root, SCNn, short ciliary nerves.

of the optic nerve (Figs. 2B and 3B) to reach the upper part of the 3.2. The otic ganglion
CG. Together with the sympathetic root (fibers from the ophthalmic
plexus) they entered the ganglion posteromedially. The short and In 16 specimens (80%), the otic ganglion occurred as a small,
much thicker parasympathetic (motor) root entered the ganglion slightly oval and flat body, approximately 1–2 mm in size. In 4 cases
posterolaterally (Fig. 3B). In all observed specimens, 4–7 mixed (20%), it had an irregular shape resembling a lentil. In all exam-
short ciliary nerves (SCNn) passed alongside the optic nerve to the ined specimens it was situated deeply in the ITF just below the
posterior pole of the eyeball and pierced it (Fig. 3A and B). foramen ovale, medial to the mandibular nerve (oval field), behind

Fig. 4. (A) The location of the otic ganglion (oval field) inside the infratemporal fossa and nearby situated neurovascular structures and muscles (inferolateral view). V/3,
mandibular nerve; CHT, chorda tympani; LN, lingual nerve; IAN, inferior alveolar nerve; IAA, inferior alveolar artery; ATN, auriculotemporal nerve; MPM, medial pterygoid;
LPM, lateral pterygoid; AM, angle of mandible; CP, coronoid process; ECA, external carotid artery and (B) The otic ganglion, the roots, and nearby situated structures
(inferolateral view). OG, otic ganglion; CHT, chorda tympani; ATN, auriculotemporal nerve (cut); MMA, middle meningeal artery (cut); V/3, mandibular nerve; LN, lingual
nerve; IAN, inferior alveolar nerve; MBrrV/3, motor branches of mandibular nerve; MPM, medial pterygoid; MV, maxillary vein. The sensory root enters the ganglion
anteromedially, the sympathetic root from below. The parasympathetic root enters the ganglion posteromedially. GGBrr/I., sensory root (ganglionic branches of mandibular
nerve); II., sympathetic root; LPN/III., parasympathetic root (lesser petrosal nerve); GPN, greater petrosal nerve; DPN, deep petrosal nerve; *, nerve exiting the otic ganglion
to join the auriculotemporal nerve.
K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211 209

the medial pterygoid and anterior to the middle meningeal artery


(Fig. 4A and B). The relatively thick sensory root entered the gan-
glion anteromedially and the parasympathetic root (with approxi-
mately the same diameter), entered it posteromedially. A very del-
icate and short sympathetic root (fibers from the plexus of the mid-
dle meningeal artery) entered the ganglion from below (Fig. 4B).
Near the otic ganglion, the greater and deep petrosal nerves
passed from the middle cranial fossa to the ITF and to the PPF. The
parasympathetic root (as the lesser petrosal nerve) reached the ITF
just medial to both the GPN and the DPN (Fig. 4B). The bundle of
fine fibers covered by these two nerves, exited the ganglion at its
upper part and joined the auriculotemporal nerve (Fig. 4B).

3.3. The pterygopalatine ganglion

The shape of the pterygopalatine ganglion correlated with the


triangular or conical shape of PPF. The 3–4 mm ganglion was tri-
angular and flat in 6 heads (30%) and conical with a broad upper
base in 14 (70%), (Fig. 6A). It was always situated below the maxil-
lary nerve inside the PPF (oval field), opposite the sphenopalatine
foramen and anterior to the pterygoid canal (Fig. 5A). The sensory
root (thicker and shorter ganglionic branches) entered the ganglion
from above and medially (Figs. 5B and 6A). Two very fine nerves;
the parasympathetic GPN (a parasympathetic root) and the sym-
pathetic DPN (a sympathetic root) reached the ganglion from the
pterygoid canal posteromedially (Fig. 6B). Fibers forming a plexus
around the maxillary artery were probably derived from the DPN
(Fig. 6B). The relatively thick greater palatine nerve (GPaN) and the
lesser palatine nerves (LPaNn) entered the ganglion from below
and anterolaterally. Just above the maxillary nerve, 2–3 fine orbital
branches were revealed entering the orbit (Fig. 6A).
We examined 60 parasympathetic ganglia (20 ciliary, 20 otic,
and 20 pterygopalatine). There was remarkable similarity among
the corresponding ganglia from side to side (right or left) and from
Fig. 5. (A) The location of the pterygopalatine ganglion (oval field) inside the ptery-
specimen to specimen in regard to their location, topography, mor-
gopalatine fossa (PPF) and nearby situated structures (lateral view). Boundaries of
phology, and configuration of their roots. the openings of communications to the PPF are marked by the symbol (curved
line). FO, foramen ovale; FR, foramen rotundum; SPF, sphenopalatine foramen;
4. Discussion V/1, ophthalmic nerve; V/2, maxillary nerve; V/3, mandibular nerve; TG, trigeminal
ganglion; GW, greater wing of sphenoid bone; LRM, lateral rectus; MA, maxillary
artery; ION, infraorbital nerve and (B) The location of the pterygopalatine ganglion,
Anatomical educational research is a dynamic field of aca- the roots, and nearby situated structures (superior view). The sensory ganglionic
demic medicine. New trends are developing in the methods of branches (pterygopalatine nerves) enter the ganglion from above and medially. PPG,
anatomical teaching; e.g. the use of more sophisticated models, pterygopalatine ganglion; V/2, maxillary nerve; GGBrr/I., sensory root (ganglionic
computer-generated images, and interactive computer programs. branches of maxillary nerve); APC, artery of pterygoid canal; MA, maxillary artery;
SPA, sphenopalatine artery; ION, infraorbital nerve; IOA, infraorbital artery; LRM,
Though there are arguments to the contrary, the strong consensus
lateral rectus.
among anatomical academics appears to be that dissection courses
remain as central tools for teaching macroscopic anatomy (Korf
et al., 2008; Hirt et al., 2010). Dissection lays a firm foundation for facial pain syndromes (du Plessis et al., 2010). Headache and facial
the development of medical language and provides a platform for pain syndromes occur in the distribution of the trigeminal nerve
developing three-dimensional anatomical knowledge. The courses branches. The mandibular nerve has an additional motor compo-
not only teach anatomical terms; they also recruit all the senses nent, which runs in a separate fascial compartment through the
of the student and thus encourage an appropriate feeling of awe ITF. Most of nerve fibers run directly to their target tissues (Leston,
and respect as the student enters his or her first encounter with an 2009). An unintended intravascular injection from an inferior alve-
actual human body for the care of which he or she is now entirely olar nerve block can result in frustrating distant complications
responsible (Böckers et al., 2010). affecting structures such as the middle ear and eyes. It can express
Perfection of surgical practice requires a precise knowledge of as a paralysis of a branch of the oculomotor nerve and the SCNn
anatomical structures, their location, and topographical relation- that innervate the ciliary muscle (Ngeow et al., 2006). A total sym-
ships. That is why gross human anatomy remains the most relevant pathetic block utilizing a combined blockade of the stellate and
basic discipline for medical students as well as surgeons. Clinically pterygopalatine ganglia is a treatment for postherpetic neural-
oriented cranial anatomy provides an understanding of the causes gia involving the ophthalmic division of the trigeminal nerve (du
of many serious problems and is essential for neurologists, neu- Plessis et al., 2010). The pterygopalatine ganglion is important for
rosurgeons, and maxillofacial surgeons, who should be especially maintaining the balance of intraocular pressure and for controlling
aware of the possible occurrence of anatomical variations and cerebral vasodilatation, which can be associated with headaches of
their clinical significance. vascular origin (Siéssere et al., 2008).
Neurovascular structures located in areas of the head that are In spite of the fact that exact mechanisms are unknown, dege-
difficult to access are often subject to disease, trauma, and other nerative changes or damage to the peripheral autonomic nervous
local or systemic conditions, e.g. cluster headaches, migraines, and system has been suggested as a possible cause of Ross syndrome.
210 K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211

Fig. 6. (A) A detail of the conical pterygopalatine ganglion and nearby situated structures (lateral view). The sensory root (ganglionic branches) enters the ganglion from above
and medially. Greater palatine nerve and lesser palatine nerves enter it from below and anterolaterally. Orbital branches reach the ganglion from above and posteromedially.
PPG, pterygopalatine ganglion; GGBrr/I., sensory root (ganglionic branches of maxillary nerve); LPaNn, lesser palatine nerves; GPaN, greater palatine nerve; OBrr, orbital
branches; IOF, inferior orbital fissure; LRM, lateral rectus and (B) roots of the pterygopalatine ganglion (posterolateral view). The sympathetic root (deep petrosal nerve) and
parasympathetic root (greater petrosal nerve) enter the ganglion from pterygoid (Vidian) canal posteromedially. PPG, pterygopalatine ganglion; V/2, maxillary nerve; ZN,
zygomatic nerve (cut); SP, sympathetic plexus of maxillary artery; APC, artery of pterygoid canal; LRM, lateral rectus, DPN/II.,sympathetic root; GPN/III., parasympathetic
root.

The syndrome consists of thermoregulatory dysfunction associ- accessory ciliary ganglion may also be located inside the orbit. It
ated with tonic pupils and areflexia, possibly the result of cranial can be readily differentiated from the ciliary ganglion proper by its
postganglionic parasympathetic and sympathetic dysfunction in location on the SCNn.
association with more widespread autonomic failure. It is not life- Sympathetic nerves also enter the orbit via the first (oph-
threatening in that patients generally learn to avoid excessive thalmic) and second (maxillary) division of the trigeminal nerve,
body heating (Ballestero-Diez et al., 2005; Hagemann and Bartke, not only as a plexus surrounding the ophthalmic artery (Thakker
2006). The harlequin sign or harlequin syndrome (terms used inter- et al., 2008). The absence of a sympathetic root has also been
changeably in the medical literature), can be similar to Ross syn- observed (Tsybul’kin, 2003). Precise understanding of the mor-
drome. They are characterized by sudden onset of hemifacial sweat- phology and function of very delicate and vulnerable orbital
ing and flushing, induced by exercise and heat, tonic pupils and structures is essential for performing safe intraorbital operations
parasympathetic oculomotor lesion. Studies by Tascilar et al. (2007) (Rene, 2006; Zhang et al., 2010) minimizing the occurrence of
report that the harlequin sign can be associated with the sympa- possible complications (Presland, 2007). The accessory oph-
thetic and parasympathetic denervation sensitivity and harlequin thalmic artery, a branch of the middle meningeal artery, enters
syndrome with occult sympathetic denervation sensitivity. the orbit through the superior orbital fissure together with the
The parasympathetic ganglia can be damaged during surgical ophthalmic or lacrimal artery. Perivascular nerves continue to
procedures in areas where they are located. In the majority of the lacrimal gland as lacrimal branches. They are presumably
cases, the ciliary ganglion is located laterally to the optic nerve, derived from the middle meningeal plexus and may include the
thus it can easily be injured by bone fragments in orbital fractures otic parasympathetic fibers (Ruskell, 2004).
and operations using the, lateral approach to the orbit. Patients The infratemporal fossa is an important anatomical region of the
should be informed before such surgery about possible develop- head for maxillofacial, craniofacial, and neurologic surgeons. It is a
ment of mydriatic or tonic (Adie‘s) pupils as a complication (Izci route to the lateral skull base and middle cranial fossa and a site
and Gönül, 2006). The surgeon should be aware that the ciliary of benign and malignant tumors originating in the nasopharynx
ganglion can rarely be located medially to the optic nerve, which and jaws. They can grow into this region, into pterygomaxillary
can complicate intraorbital procedures (Girijavallabhan and Bhat, space or fissure (Auluck et al., 2007; Roberti et al., 2007). The ptery-
2008). The ciliary ganglion can be a landmark during surgery in the gomaxillary fissure represents a major pathway for spreading of
orbit. Pushing the adipose and connective tissue surrounding the inflammatory or neoplastic processes to the respective compart-
ganglion medially can prevent its injury (Zhang et al., 2010). Also ments, therefore, this space represents a common cavity in the
the relationship between the dimension, shape, and topography of skull-base and the face. Its neurovascular contents and communi-
the ciliary ganglion and skull has clinical significance. Tsybul’kin cation pathways make them crucial in odontostomatology (Auluck
(2003) states that the position postero-inferior to the optic nerve et al., 2007).
is typical of brachycephaly, while the antero-superior position is The petrosal nerves can be valuable landmarks during surgical
typical of dolichocephaly. procedures involving the middle cranial fossa (Tubbs et al., 2009)
Sinnreich and Nathan (1981) report that, in some cases, the and ITF. The relationships of the lesser petrosal nerve to surround-
parasympathetic root is missing and the ciliary ganglion is attached ing structures have been described by Kakizawa et al. (2007), but
directly to the inferior branch of the oculomotor nerve or the fibres its course has not been well understood. It may be confused with
innervating the inferior oblique. Several authors reported that the the greater and deep petrosal nerves (Fig. 4B). We were not able
K. Lovasova et al. / Annals of Anatomy 195 (2013) 205–211 211

to find any studies focused on the course and topography of these References
nerves in the ITF before their entrance to the PPF. For all these rea-
sons, anatomical knowledge on the ITF and the nerves it contains Auluck, A., Shetty, S., Desai, R., Mupparapu, M., 2007. Recurrent ameloblastoma of
the infratemporal fossa: diagnostic implications and a review of the literature.
is essential for choosing the best possible surgical approach to this Dentomaxillofac. Radiol. 36, 416–419.
area (Isolan et al., 2007). Ballestero-Diez, M., Garcia-Rio, I., Dauden, E., Corrales-Arroyo, M.J., Garcia-Diez,
Surgical access to the PPF is difficult as well. The nerves and A., 2005. Ross syndrome, and entity included within the spectrum of partial
dysautonomic syndromes. JEADV 19, 729–731.
their bony foramina (e.g. the Vidian and maxillary nerves), are cru- Böckers, A., Jerq-Bretzke, L., Lamp, C., Brinkmann, A., Traue, H.C., Böckers, T.M., 2010.
cial anatomical landmarks in identifying the maxillary and internal The gross anatomy course: an analysis of its importance. Anat. Sci. Educ. 3,
carotid arteries at the skull base (Fortes et al., 2008). There may 3–11.
Fortes, F.S., Sennes, L.U., Carrau, R.L., Brito, R., Ribas, G.C., Yasuda, A., Rodrigues, A.J.,
be a dual sympathetic pathway through the Vidian nerve and the Sniderman, C.H., Kassam, A.B., 2008. Endoscopic anatomy of the pterygopalatine
periarterial plexuses along the maxillary artery inside the PPF. fossa and the transpterygoid approach: development of a surgical instruction
Both pathways – the internal carotid artery, Vidian nerve and the model. Laryngoscope 118, 44–49.
Girijavallabhan, V., Bhat, K.M.R., 2008. Positional variation of the ciliary ganglion
external carotid artery – maxillary plexus, reinforce the maxillary
and its clinical relevance. Neuroanatomy 7, 38–40.
sympathetic plexus (Fig. 6B), (Rusu and Pop, 2010). The Vidian canal Hagemann, G., Bartke, T., 2006. Adie’s pupil in the Ross syndrome. URL:
has become an important landmark in surgical approaches to the http://www.nejm.org/doi/full/10.1056/NEJMicm040986 (accessed January
skull base (Osawa et al., 2009; Tubbs et al., 2009). The surgery can be 2011).
Hirt, B., Shiozawa, T., Herlan, S., Wagner, H.J., Küppers, E., 2010. Surgical prosection
rather risky due to varying relationship of this canal to the sphenoid in a traditional anatomical curriculum – Tübingens’ Sectio chirurgica. Ann. Anat.
sinus (Yazar et al., 2007). This area of the skull base represents only 192, 349–354.
one example in which computed tomography (CT) and magnetic Isolan, G.R., Rowe, R., Al-Mefty, O., 2007. Microanatomy and surgical approaches to
the infratemporal fossa: an anaglyphic three-dimensional stereoscopic printing
resonance imaging (MRI) are invaluable tools for preoperatively study. Skull Base 17, 285–302.
delineating the anatomy of the area in which surgery is planned Izci, Y., Gönül, E., 2006. The microsurgical anatomy of the ciliary ganglion and its
(Leblanc, 1992). clinical importance in orbital traumas: an anatomic study. Minim. Invasive Neu-
rosurg. 49, 156–160.
Regarding the location of the three cranial parasympathetic Kahle, W., Frotscher, M., 2002. Nervous system and sensory organs. Color Atlas and
ganglia presented here, our results are in accordance with the Textbook of Human Anatomy, fifth ed. Georg Thieme Verlag, Stuttgart.
observations that have appeared in the literature (Kahle and Kakizawa, Y., Abe, H., Fukushima, Y., Hongo, K., El-Khouly, H., Rhoton, A.L., 2007. The
course of the lesser petrosal nerve on the middle cranial fossa. Neurosurgery 61,
Frotscher, 2002; Lanz and Wachsmuth, 2004; Izci and Gönül, 2006; 15–23.
Siéssere et al., 2008). However, the aim of our study was not Korf, H.-W., Wicht, H., Snipes, R.L., Timmermans, J.-P., Paulsen, F., Rune, G., Baumgart-
only to confirm the location and general topography of these Vogt, E., 2008. The dissection course – necessary and indispensable for teaching
anatomy to medical students. Ann. Anat. 190, 16–22.
three ganglia. Our primary goal was to contribute to the body of
Lanz, T., Wachsmuth, W., 2004. Kopf: Übergeordnete Systeme, Teil A Formen-
anatomical knowledge much more specific information about these twicklung des Kopfes, Teil B Gehirn-und Augenschädel. Praktische Anatomie,
parasympathetic ganglia – detailed photographic documentation Springer-Verlag, Sonderausgabe.
concerning the configuration and relationships of their sensory, Leblanc, A., 1992. Anatomy and Imaging of the Cranial Nerves. A Neuroanatomic
Method of Investigation Using Magnetic Resonance Imaging (MRI) and Com-
sympathetic, and parasympathetic roots as well as their relation- puted Tomography (CT). Springer-Verlag, Berlin.
ship to other important neural and vascular structures in the orbital Leston, J.M., 2009. Functional anatomy of the trigeminal nerve. Neurochirurgie 55,
apex and skull base. 99–112.
Ngeow, W.C.H., Shim, C.H.K., Chai, W.L., 2006. Transient loss of power of accommo-
We were motivated to carry out this study having been unable dation in 1 eye following inferior alveolar nerve block: report of 2 cases. J. Can.
to find any detailed photographs in the anatomical literature or Dent. Assoc. 72, 927–931.
even detailed descriptions of the relationships of the sensory, sym- Osawa, S., Rhoton, A.L., Seker, A., Shimizu, S., Fujii, K., Kassam, A.B., 2009.
Microsurgical and endoscopic anatomy of the Vidian canal. Neurosurgery 64,
pathetic, or parasympathetic roots to the ganglia, to each other, or 385–411.
to other neural and vascular structures in their vicinity. This study du Plessis, M., Navsa, N., Bosman, M.C., 2010. Preliminary results on a study to locate
provides a full anatomical view of the topography and morphology the pterygopalatine fossa using mathematical formulae. Clin. Anat. 23, 931–935.
Presland, A., 2007. Applied ocular physiology and anatomy. Anaesth. Intens. Care
of many structures thus far incompletely displayed in anatomical Med. 8, 379–382.
medical textbooks and atlases. The anatomical details displayed Rene, C., 2006. Update on orbital anatomy. Eye 20, 1119–1129.
by our investigation strongly suggests that dissection is still an Roberti, F., Boari, N., Mortini, P., Caputy, A.J., 2007. The pterygopalatine fossa: an
anatomic report. J. Craniofac. Surg. 18, 586–590.
important part of teaching anatomy and provides an excellent
Ruskell, G.L., 2004. Distribution of pterygopalatine ganglion efferents to the lacrimal
opportunity for the integration of anatomy and clinical medicine. gland in man. Exp. Eye Res. 78, 329–335.
Rusu, M.C., Pop, F., Curcă, G.C., Podoleanu, L., Voinea, L.M., 2009. The ptery-
Conflict of interest statement gopalatine ganglion in humans: a morphological study. Ann. Anat. 191,
196–202.
Rusu, M.C., Pop, F., 2010. The anatomy of the sympathetic pathway through the
The authors declare that they have no conflict of interest. pterygopalatine fossa in humans. Ann. Anat. 192, 17–22.
Siéssere, S., Vitti, M., de Sousa, L.G., Semprini, M., Iyomasa, M.M., Regalo, S.C.H.,
Acknowledgments 2008. Anatomic variation of cranial parasympathetic ganglia. Braz. Oral Res. 22,
101–105.
Sinnreich, Z., Nathan, H., 1981. The ciliary ganglion in man (anatomical observation).
The authors would like to express their gratitude to reviewers Anat. Anz. 150, 287–297.
for valuable comments aimed to improve the study. They also thank Tascilar, N., Tekin, N.S., Erdem, Z., Alpay, A., Emre, U., 2007. Unnoticed dysau-
Katarina Bodnarova from Oakland Community College, Auburn tonomic syndrome of the face: harlequin syndrome. Auton. Neurosci. 137,
1–9.
Hills, Michigan for graphic processing of presented figures (original
Thakker, M.M., Huang, J., Possin, D.E., 2008. Human orbital sympathetic nerve path-
pen and ink drawings), (Fig. 1A–C) and Prof. W. Bradford DeLong, ways. Ophthal. Plast. Reconstr. Surg. 24, 360–366.
MD, from the Department of Neurosurgery, University of California, Tsybul’kin, A.G., 2003. Individual variability of external structure and topography of
human ciliary ganglion. Morfologia 124, 34–37.
San Francisco for English-language proofreading of this article.
Tubbs, R.S., Custin, J.W., Salter, E.G., Sheetz, J., Zehren, S.J., Oakes, W.J.,
This study was supported by the Grants KEGA 3/7291/09 and 2005. Landmarks for the greater petrosal nerve. Clin. Anat. 18,
006UPJS-4/2011. 210–214.
Tubbs, R.S., Menendez, J., Loukas, M., Shoja, M.M., Shokouhi, G., Salter, E.G.,
Cohen-Gadol, A., 2009. The petrosal nerves: anatomy, pathology, and surgical
Appendix A. Supplementary data considerations. Clin. Anat. 22, 537–544.
Yazar, F., Cankal, F., Haholu, A., Kilic, C., Tekdemir, I., 2007. CT evaluation of the Vidian
Supplementary data associated with this article can be canal localization. Clin. Anat. 20, 751–754.
found, in the online version, at http://dx.doi.org/10.1016/ Zhang, Y., Liu, H., Liu, E.Z., Lin, Y.Z., Zhao, S.G., Jing, G.H., 2010. Microsurgical anatomy
of the ocular motor nerves. Surg. Radiol. Anat. 32, 623–628.
j.aanat.2013.01.011.

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