Three-Dimensional Interactive Atlas of Cranial Nerve-Related Disorders

Abstract

Anatomical knowledge of the cranial nerves (CN) is fundamental in education, research and clinical practice. Moreover, understanding CN-related pathology with underlying neuroanatomy and the resulting neurological deficits is of vital importance. To facilitate CN knowledge anatomy and pathology understanding, we created an atlas of CN-related disorders, which is a three-dimensional (3D) interactive tool correlating CN pathology with the underlying surface and sectional neuroanatomy as well as the resulting neurological deficits. A computer platform was developed with: 1) anatomy browser along with the normal brain atlas (built earlier); 2) simulator of CN lesions; 3) tools to label CN-related pathology; and 4) CN pathology database with lesions and disorders, and the resulting signs, symptoms and/or syndromes. The normal neuroanatomy comprises about 2,300 3D components subdivided into modules. Cranial nerves contain more than 600 components: all 12 pairs of cranial nerves (CN I – CN XII) and the brainstem CN nuclei. The CN pathology database was populated with 36 lesions compiled from clinical textbooks. The initial view of each disorder was preset in terms of lesion location and size, surrounding surface and sectional neuroanatomy, and disorder and neuroanatomy labeling. Moreover, path selection from a CN nucleus to a targeted organ further enhances pathology-anatomy relationships. This atlas of CN-related disorders is potentially useful to a wide variety of users ranging from medical students and residents to general practitioners, neuroradiologists and neurologists, as it contains both normal brain anatomy and CN-related pathology correlated with neurological disorders presented in a visual and interactive way.

Introduction

Anatomical knowledge of the cranial nerves (CN) and their nuclei is fundamental in education, research and clinical practice. In addition, understanding CN-related (and, generally, any brain-related) pathology with underlying neuroanatomy and the resulting neurological deficits is of vital importance. Therefore, one of our major goals is to create a 3D interactive atlas of neurological disorders able to provide the correspondence between damage to any cerebral location with the resulting disorders. Towards this objective, we have already built a 3D Stroke Atlas¹ providing this correspondence for cerebrovascular lesions. This work extends our previous effort towards CN pathology.

The atlas of CN-related disorders is a three-dimensional (3D) interactive tool correlating CN pathology with the underlying neuroanatomy and the resulting neurological deficits. It contains a 3D, parcellated, labeled and explor-able atlas of normal neuroanatomy along with a pathology database. Normal neuroanatomy, available in the brain atlas, is subdivided into about 2,300 components and contains cerebrum, cerebellum, brainstem, spinal cord, arteries, veins, dural sinuses, tracts, cranial nerves, white matter, deep gray nuclei, ventricles, visual system, muscles and glands. The pathology database comprises synthesized CN lesions providing disorder-localization relationships, such that each lesion is labeled with the disorder and the resulting signs, symptoms, and/or syndromes. These relationships are compiled from the literature.

However, literature descriptions typically do not specify the lesion size, shape, and location. Therefore additionally to the abovementioned approach, the assessment of a resulting deficit may be facilitated visually by presenting the complete “anatomical path” from a CN nucleus to a CN nerve with its branches to a targeted muscle or muscles/organs. Then, placing a virtual lesion mentally on the anatomical path allows the investigator to observe which part of this path (and potentially other paths depending on the size of the lesion) will be affected. And conversely, having identified a damaged muscle with all the anatomical paths supplying it could facilitate a potential localization of the lesion. The anatomical path concept for the cranial nerves, enabled by brain compositing and decompositing operations available in the brain atlas, is implemented here.

Material and method

In order to create the atlas of CN-related disorders, we used an approach employed earlier to build the Stroke Atlas¹ The Stroke Atlas is a 3D interactive tool, which correlates cerebrovascular pathology with the underlying neuroanatomy and the resulting neurological deficits. It is based on a 3D brain atlas of normal anatomy created from 3 and 7 Tesla scans and described in detail earlier^2-6. The normal neuroanatomy is subdivided into modules⁶, and the module with the cranial nerves contained (originally) 440 components: all 12 pairs of cranial nerves (CN I - CN XII) and the brainstem CN nuclei⁵.

The main components of the Stroke Atlas reused and extended here are: 1) atlas of normal surface and sectional neuroanatomy along with anatomy browser; 2) simulator of cerebral pathologies; 3) tools to label pathology; and 4) pathology database. Surface neuroanatomy is presented in the form of about 2,300 3D components represented as polygonal objects. Sectional neuroanatomy is presented in the form of axial, coronal, and/or sagittal MR tripla-nar displayed as 3D textures. The anatomy browser enables the user to make rapid brain compositing and decompositing from individual and/or group components with a few clicks, and to study the composite from any angle and at a wide range of magnifications.

The pathology database correlates lesions with the resulting disorders. Each disorder is described in terms of the corresponding signs, symptoms and/or syndromes. In order to model CN pathology in 3D, a lesion was depicted as a white sphere and pathology along a CN as a white dilated cylinder. An index correlating neuroanatomy with CN pathology was structured as a list, which is hierarchical with respect to anatomy and linear with respect to disorders. For each disorder, a sub-list of signs, symptoms and/or syndromes was compiled from materials reported in the literature^7-9. The initial view of each disorder was preset in terms of lesion location and size, surrounding surface and sectional neuroanatomy, and lesion and neuroanatomy labeling.

To enable the investigator to make a visual assessment of muscle-CN relationships, the existing CN module⁵ was extended and enhanced in terms of branching patterns, nerve course, anatomical index, number of branches, and branch length. The course of cranial nerve branches was lengthened to reach the targeted muscles/organs or edited to have more precise entry location. Several new nerve and branch names were added into the anatomical index. Moreover, 163 new CN branches were created (37% increase in the number of CN components), mostly of the facial nerve. There is a great variation regarding branching patterns and the number of branches¹⁰,¹¹. Therefore, the branching patters were updated in the atlas to correspond to the most frequent patterns described in the literature. The temporal branch was partitioned in the atlas into anterior and posterior branches below the zygomatic arch, as it usually divides in this way¹¹ (the temporal branch courses along the zygomatic system as one (14%), two (57%), three (14%) or four (14%) branches¹²). There are generally multiple zygomatic branches¹¹ and two branches were created in our atlas. The buccal and cervical branches are usually single¹¹ and they remain single in the atlas. Two marginal mandibular branches were implemented in the atlas, as there are typically two of them¹¹ (this branch may have one (21%), two (67%), three (9%) or four (3%) major branches¹³). The course of several nerves and branches was edited to run on the superficial or deep surface of the innervated muscle. The nerve entry locations, when available, were also edited. The CN-muscle relationships were compiled from the following sources^10-18.

Results

A hierarchical index of anatomy integrated with a linear index of CN disorders was constructed (see Appendix for the list of disorders and Figure 1 for the sub-lists of signs, symptoms and/or syndromes for individual CN lesions). The disorder database was populated with 36 CN lesions (meaning that, on average, there are three lesions per CN). The views and labeling of all CN-related lesions were preset. Examples of CN pathology correlated with the resulting disorder and the surrounding surface and sectional neuroanatomy for all 12 pairs of the cranial nerves are illustrated in Figure 1.

Figure 1.

Illustration of CN pathology correlated with the resulting disorder and the surrounding surface and sectional neuroanatomy. The images are composed by means of the anatomy browser which provides: 1) exploration operations for 3D display and manipulation (rotate, zoom, pan, and set view), 2) brain compositing/decompositing of individual components and/or group selection, 3) two-way (3D view-index) mapping, 4) 3D labeling and component highlighting, 5) 3D brain cutting in 7 directions, and 6) axial/coronal/sagittal MR (magnetic resonance) triplanar display. The orientation box in the top-left corner provides the viewing direction (S — superior, I — inferior, A — anterior, P — posterior, L — left, and R — right). a) CN I; b) CN II; c) CN III; d) CN IV; e) CN V; f) CN VI; g) CN VII; h) CN VIII; i) CN IX; j) CN X; k) CN XI; 1) CN XII.

The CN-muscle correlation (with the state-of-the-art review and as implemented in the atlas) is presented in Table 1. The extended facial nerve and the facial muscles along with all the cranial nerves are illustrated in Figure 2.

Table 1.

Muscle-CN correlation (options/conditions in italics are implemented in our atlas).

Muscles	Cranial nerves
Auricularis anterior	Posterior rami of temporal branch of CN VII4 p22. Temporal branches of CN VII7 p619,8 pl368.
Auricularis posterior	Posterior auricular branch of CN VII7 p619,8 pl247,8 pl368. Posterior auricular nerve of CN VII6 p79. Auricular branch of posterior auricular nerve of CN VII8 pl246.
Auricularis superior	Temporal branches of CN VII7 p619,8 pl368.
Buccinator	Buccal branch of CN VII7 p487. Innervated from the superficial surface3 p97.
Corrugator supercilii	Temporal branches of CN VII5 pl03,7 p486. Temporal (frontal) branch of CN VII innervates the transverse head and a zygomatic-buccal branch of CN VII supplies the oblique head via a lower eyelid and medial canthus4 p8. Pierced by supratrochlear nerve of V1 of CN V4 p40.
Depressor anguli oris	Buccal and marginal mandibular branches of CN VII3 p97,7 p487. Innervated from the deep surface3 p97.
Depressor labii inferioris	Marginal mandibular branch of CN VII5 pl03,7 p487. Innervated from the deep surface3 p97.
Depressor septi nasi	Buccal and sometimes zygomatic branches of CN VII7 p549. Zygomatic branches of CN VII6 pl03.
Depressor supercilii	Zygomatic-buccal branch of CN VII via a lower eyelid and medial canthus4 p8. Temporal or zygomatic-buccal branch of CN VII4 p9.
Inferior oblique	Branch to inferior oblique enters the muscle on the interconal surface at its mid-position4 pll9.
Inferior rectus	Inferior branch of CN III enters the superior surface7 p660. Motor nerve enters at the junction of the posterior one third and anterior two thirds of the muscle4pll9.
Lateral pterygoid	Lateral pterygoid nerve of V3 of CN V enters the deep surface of the muscle1 p51. Buccal nerve of V3 passes through it (between the two heads)8 pl237. Lateral pterygoid nerve, a branch of V3 of CN V6 p48. Buccal nerve of V3 innervates the upper head and the lateral part of the lower head; a branch arising from V3 supplies medial part of the lower head7 p539. Branch from anterior trunk of V3 of CN V8 p801.
Lateral rectus	Abducens nerve (CN VI) enters the medial surface7 p660. Motor nerve enters at the junction of the posterior one third and anterior two thirds of the muscle4 pll9.
Levator anguli oris	Zygomatic and buccal branches of CN VII7 p486. Innervated from the superficial surface3 p97.
Levator labii superioris	Zygomatic and buccal branches of CN VII7 p486. Innervated from the deep surface3 p97.
Levator labii superioris alaeque nasi	Zygomatic and superior buccal branches of CN VII7 p549.
Levator palpebrae superioris	Superior branch of CN III enters the inferior surface1 p659.
Masseter	Masseteric nerve of V3 of CN V1 p50,7 p538.
Medial pterygoid	Medial pterygoid nerve of V3 of CN V1 p50.
Medial rectus	Inferior branch of CN III enters the lateral surface1 p660. Motor nerve enters at the junction of the posterior one third and anterior two thirds of the muscle4 pll9.
Mentalis	Marginal mandibular branch of CN VII5 pl03,7 p486. Innervated from the superficial surface3 p97.
Nasalis, alar part	Buccal and sometimes zygomatic branches of CN VII7 p549. Zygomatic branches of CN VII5 pl03.
Nasalis, transverse part	Buccal and sometimes zygomatic branches of CN VII7 p549. Zygomatic branches of CN VII5 pl03.
Occipitofrontalis, frontal belly	Temporal branches of CN VII5 pl03,7 p481. Anterior and middle rami of temporal branch of CN VII4 p22. Penetrated medially by supratrochlear nerve of V1 of CN V4 p40. Temporal branches enter undersurface of the muscle2 p80.
Occipitofrontalis, occipital belly	Posterior auricular nerve of CN VII7 p481. Occipital branch of posterior auricular nerve of CN VII5 p103.
Orbicularis oculi	Temporal and zygomatic branches of CN VII5 pl03,7 p482. Temporal or zygomatic-buccal branch of CN VII supplies the medial superior portion via a lower eyelid and medial canthus4 p9. Anterior and middle rami of temporal branch of CN VII supply the superior portion4 p22. Zygomatic branches cross the zygomatic bone to the lateral canthus supplying the or bicular is oculi8pl247. Innervated from the deep surface3 p97. Zygomaticofacial nerve of V2 of CN V perforates orbicularis oculi7 p494.
Orbicularis oris	Buccal and mandibular branches of CN VII7 p488. Zygomatic branches supply the superior portion and buccal branches the inferior portion5 pl03. Buccal branches3 p97. Lower buccal and marginal mandibular branches of CN VII8 p798.
Palatine tonsil	Tonsillar branches of CN IX1 pl49.
Posterior belly of digastric	Digastric branch of CN VII1 p85.
Procerus	Temporal and lower zygomatic branches of CN VII7 p549. Temporal branch or lower zygomatic-buccal branch via the lower eyelid and medial canthus4 p7. Temporal branch supplies the upper portion5 pl03, (at times)4 p22. Temporal branch3 p97.
Risorius	Buccal branches of CN VII5 pl03,7 p488,8 p799. Innervated from the deep surface3 p97.
Sternocleidomastoideus	External branch of CN XI1 pl73.
Superior oblique	Trochlear nerve (CN IV) enters the superior surface7 p660. CN IV enters as 3 or 4 rootlets that penetrate the upper border of the muscle along its posterior third (the only extraocular nerve that does not penetrate the conal surface of its muscle)4 pl35.
Superior rectus	Superior branch of CN III enters the inferior surface7 p660. Motor nerve enters at the junction of the posterior one third and anterior two thirds of the muscle4 p119.
Temporalis	Deep temporal nerves of V3 of CN V1 p50,7 p538. The anterior deep temporal nerve is frequently a branch of the buccal nerve of V38 pl237.
Temporoparietalis	Posterior rami of temporal branch of CN VII4 p22.
Tongue	Lingual nerve of V3 of CN V (anterior two thirds of the tongue)1 p51. Corda tympani of CN VII (taste sensation, anterior two thirds of the tongue)1 p86. Lingual branches of CN IX (to posterior one third of the tongue (sensory and taste)1 pl49. Hypoglossal nerve (CN XII)1 pl83.
Trapezius	External branch of CN XI1 pl73.
Zygomaticus major	Zygomatic and buccal branches of CN VII3 p97,7 p486. Zygomatic branches of CN VII5 p103. Innervated from the deep surface3 p97.
Zygomaticus minor	Zygomatic and buccal branches of CN VII7 p486. Zygomatic branches of CN VII5 p103. Buccal branches of CN VII3 p97. Innervated from the deep surface3 p97.

¹Binder D, Sonne DC, Fischbein NJ Cranial nerves: anatomy, pathology, imaging. Stuttgart-New York: Thieme; 2010.

²Larrabee WF, Makielski KH, Henderson JL. Surgical anatomy of the face. 2^nd ed. Philadelphia: Lippincott Williams & Wilkins; 2003.

³May M, Schaitkin B. The facial nerve: May's second edition. New York, Stuttgart: Thieme; 2000.

⁴Jordan DR, Mawn L, Richard L, et al. Surgical anatomy of the ocular adnexa: a clinical approach. 2^nd ed. New York: 5 Oxford University Press; 2012.

⁵Netter FH. The Ciba collection of medical illustrations, Volume 1: Nervous system, Part 1: Anatomy and physiology. West Caldwell, NJ: Ciba-Geigy; 1991.

⁶Schuenke M, Schulte E, Schumacher U. Atlas of anatomy. head and neuroanatomy. Stuttgart-New York: Thieme; 2008.

⁷Standring S. Gray's Anatomy. The anatomical basis of clinical practice. 40^th ed. Oxford: Churchill Livingstone; 2008.

⁸Williams PL. Gray's Anatomy. The anatomical basis of medicine and surgery. 38^th ed. Oxford: Churchill Livingstone; 1995

Figure 2.

Facial muscles — CN spatial relationships. A) The extended facial nerve. B) The facial muscles along with all cranial nerves.

Discussion

The atlas of CN-related disorders correlates localized CN pathology with both the resulting disorder and the surrounding neuroanatomy. It also provides a 3D interactive display both of labeled pathology and neuroanatomy, freely composed by the investigator. Disorders are described in terms of the resulting signs, symptoms and/or syndromes, and they have been compiled for each pair of the cranial nerves as well as for some groups of them. The preset views with labeled pathology and neuroanatomy facilitate and expedite the use of this atlas, while allowing the investigator to quickly update the studied 3D scene, if needed. Path selection from a CN nucleus to a targeted organ further enhances pathology-anatomy relationships. To the best of our knowledge, this is the first 3D, interactive atlas of CN-related disorders. The atlas is potentially useful for medical students, residents, general practitioners, neuroradiologists and neurologists, as it contains both normal brain anatomy and CN-related pathology correlated with disorders presented in a visual and interactive way.

This atlas has limitations in terms of the accuracy of pathology modeling and the size of the pathology database. In order to model pathology, we used spheres (to model lesions) and dilated cylinders (to model pathology along cranial nerves). However, actual pathology may be much more complex and it often distorts patient's neuroanatomy.

The current CN pathology database contains 36 lesions. We were able to compile the complete disorder index covering deficits of each of 12 pairs of the cranial nerves along with their nuclei and some multiple cranial nerve deficits based on only three textbooks. Although increasing the number of sources would provide more materials, this would also potentially increase material inconsistency. On average, there are three lesions per cranial nerve and the largest number of lesions (i.e., 14) is set in the CN II (generally, in the visual system). The materials on locations of lesions in the visual system and the resulting deficits are also the most consistent across the textbooks used here. Some of CN-related deficit descriptions are complementary across these sources and they were combined here. In the case of differences (such as lesions of the CN VII), we used a single source.

Anatomical descriptions, however, are often contradictory and confusing, partly because of the inconsistent nomenclature¹⁰. Moreover, many past anatomical studies used preserved cadaveric heads and structures were more difficult to separate and identify¹⁰. We also observe a discrepancy between the courses of the facial nerve branches in our atlas (based on the textbook descriptions) and those presented in several drawings. Here, we referred to multiple sources to deal with these inconsistencies, and the configurations implemented in the atlas are indicated in Table 1.

The relationships between the head muscle and the cranial nerves available in the atlas correspond to the usual branching patterns, however, the current version of the atlas does not contain any variants. Moreover, despite creating more than 600 CN segments, this CN network is still oversimplified to balance between the complexity of the cerebral model and the performance of the application.

Conclusions

The atlas of CN-related disorders is a new tool which provides disorder-localization relationships along with neuroanatomy exploration. It presents various CN pathology situations in 3D labeled with the resulting disorders and associated signs, symptoms and/or syndromes along with the surrounding neuroanatomy par-cellated into about 2,300 components, including more than 600 CN-related components. The atlas is potentially useful to a wide variety of users ranging from medical students and residents to general practitioners, neuroradiologists and neurologists, as it contains both normal brain anatomy and CN-related pathology correlated with neurological disorders presented in a visual and interactive way.

Appendix

Neuroanatomy — CN pathology index, hierarchical with respect to anatomy and linear with respect to disorders (in italics).

• Olfactory nerve (CN I)

  • -Smell disturbances

• Optic nerve (CN II)/Visual system

  • -Complete lesions of the optic nerve
  • -Partial lesions of the optic nerve
  • -Optic nerve ischemia
  • -Junctional optic nerve-chiasm lesions
  • -Centrally-located lesions of the optic chiasm
  • -Laterally-located lesions of the optic chiasm
  • -Optic tract lesions
  • -Lateral geniculate body lesions
  • -Anterior temporal lobe lesions of the optic radiation
  • -Parietal or occipital lobe lesions of the optic radiation
  • -Temporoparietal lobe lesions of the optic radiation
  • -Lesions of the upper bank of the calcarine cortex
  • -Lesions of the lower bank of the calcarine cortex
  • -Lesions of the entire calcarine cortex

• Oculomotor nerve (CN III)

  • -Oculomotor nerve palsy

• Trochlear nerve (CN IV)

  • -Trochlear nerve palsy

• Trigeminal nerve (CN V)

  • -Trigeminal neuralgia
  • -Corneal reflex absence

• Abducens nerve (CN VI)

  • -Abducens nerve palsy

• Oculomotor and abducens nerves (CN III, VI)

  • -Supranuclear palsy of conjugate horizontal gaze
  • -Nuclear palsy of conjugate horizontal gaze
  • -Internuclear palsy of conjugate horizontal gaze

• Facial nerve (CN VII)

  • -Lesions distal to the stylomastoid foramen
  • -Lesions within the facial canal proximal to the chorda tympani
  • -Lesions within the internal auditory meatus
  • -Hemifacial spasm

• Vestibulocochlear nerve (CN VIII)

  • -Lesion of CN VIII
  • -Glossopharyngeal nerve (CN IX)
  • -Lesion of CN IX
  • -Glossopharyngeal neuralgia

• Vagus nerve (CN X)

  • -Unilateral lesions of the nucleus ambiguus

• Accessory nerve (CN XI)

  • -Accessory nerve palsy

• Hypoglossal nerve (CN XII)

  • -Hypoglossal nerve palsy

• Multiple cranial nerve deficits

  • -Foster Kennedy syndrome (CN I, II)
  • -Cavernous sinus syndrome (CN III, IV, V1, V2, VI)
  • -Cerebellopontine angle syndrome (CN V, VII, VIII)