The Vestibuloocular Reflex and the Yoked Extraocular MusclesArvind Kumar, MD1,2, Richard Gacek, MD3, Philip Littlefield, MD1,4

1Department of Otolaryngology, Feinberg Medical School, Northwestern University, Chicago, IL2Ear Institute of Chicago, LLC., Hinsdale, IL

3Department of Otolaryngology, University of Massachusetts Medical School, Worcester, MA4Department of Surgery, Walter Reed Army Medical Center, Washington, DC

AbstractProblem Addressed:The neuroanatomy of the vestibuloocular reflex (VOR) and the anatomy and function of the yoked extraocular muscles are complex. Descriptions of the whole VOR are scattered in the literature of several different disciplines. The purpose of this poster is to provide a conceptual framework of the anatomy of the various nuclear groups involved in the VOR, delineate their connections, and to describe the anatomy of yoked eye muscles and their function following utriculopetal and utriculofugal deflections of the canal cupulae.Methods and Measures:The English world literature on this subject was identified by entering appropriate keywords into MEDLINE from 1966 to date. The selection of the articles was based on their relevance to the subject. Data was extracted from review articles on this subject, from papers that described the experimental delineation of nuclear groups of the VOR, as well as from clinical case reports describing VOR deficits resulting from brainstem lesions.Results:Unilateral stimulation of the semicircular canals results in conjugate eye movements even though the innervation of each set of extraocular muscles is unilateral. This is because the VOR pathways cross, and because of the horizontal and vertical gaze centers, the PPRF and the riMLF. A detailed description of all nuclear groups and pathways are provided.Conclusions:Stimulation of any semicircular canal results in conjugate eye movements.Clinical Significance of Study:Theories regarding the mechanisms of benign paroxysmal positional vertigo should be unified with these concepts.

This work was supported by the Center for Hearing Restoration and Ear Research, Hinsdale, IL.

MethodsThe published world literature in English on this subject was identified by entering appropriate key words into MEDLINE from 1966 to date. The selection of the articles was based on their relevance to the subject. Data were extracted from review articles, articles describing experimental delineation of VOR nuclear groups and pathways, and from clinical case reports describing VOR deficits.

Results♦Ampullar anatomy:

♦ The ampullated end of each SD is partitioned by solid ridge, the crista ampullaris.

♦ Vestibular hair cells are located on the surface of the crista.♦ Stereocilia and kinocilia of the hair cells project into the cupula.♦ The kinocilia of the horizontal SD face the utricle.♦ The kinocilia of vertical SDs face the canal.

♦Cupular physiology:♦ Vestibular neurons have a resting discharge of ~90 spikes/s.♦ Horizontal SD - deflection of the cupula towards the utricle (ampullopetal)

causes upregulation of discharge, and deflection of cupula towards the canal (ampullofugal) causes downregulation.

♦ Vertical SD - deflection of the cupula towards the non-utricular side of the SD (ampullofugal) causes upregulation of discharge, while deflection of the cupula towards the utricular side (ampullopetal) causes downregulation.

Anatomy of right horizontal SD afferents – the slow phase of horizontal nystagmus (Figure 2):♦Path 1: Right VN afferents → cross midline → left VIth nerve nuclear motor

neurons → left VIth nerve → left lateral rectus (LR).♦Path 2: Right VN afferents → cross midline → left VIth nerve nucleus

(abducens internuclear neurons) → cross midline and ascend in the right medial longitudinal fasciculus (MLF) → right IIIrd nerve nucleus (medial rectus subnucleus) → right IIIrd nerve → right medial rectus (MR).

♦The left LR and the right MR contract simultaneously – the eyes to drift to the person’s left.

IntroductionDescriptions of the VOR and the conjugate actions of the yoked eye muscles are scattered throughout the literature of several disciplines. A single comprehensive account of cupular mechanics, the VOR, and the function of the yoked eye muscles is not readily available. The purpose of this poster is to provide a conceptual framework of cupular mechanics, the anatomy of the various nuclear groups involved in the VOR (Figure 1), delineate their connections, and describe the anatomy of yoked eye muscles and their function during individual semicircular duct (SD) stimulation.

The fast phase of horizontal nystagmus2 (Figure 3):♦Right VN afferents → Burster-driving neurons (BDNs) in the left nucleus

prepositus hypoglossi (PH) → excitatory burst neurons (EBNs) in the right paramedian pontine reticular formation (PPRF) → both populations of the right VIth nerve nucleus.

♦Path 1: Right abducens internuclear neurons → cross midline and ascend in the left MLF → MR subnucleus of the left IIIrd nerve nucleus → left IIIrd nerve → left MR.

♦Path 2: Right abducens motor neurons → right VIth nerve → right LR.♦Fast phase of eye movement - to the person’s right.

Actions of the yoked muscles that cause vertical and torsional eye movements3,4:♦ Inferior rectus (IR): With the eye in the primary position, the visual axis

makes an angle of 23° with the orbital axis and the axis of the IR. Because of this angle and its position of insertion, from the primary position, the inferior rectus depresses and extorts (outward rotation of the superior limbus away from the nose) the globe (Figure 5).

♦Superior oblique (SO): With the eye in the primary position, the SO forms an angle of 54° with the visual axis. From the primary position, the main action of SO is intorsion of the globe (inward rotation of the superior limbus towards the nose). Secondary actions are depressionand abduction (Figure 6).

♦Superior rectus (SR): With the eye in the primary position, the SR forms an angle of 23° with the visual axis. The primary action in this position is elevation. Because of its angle and position of insertion, it also intorts and adducts the globe (Figure 7).

♦ Inferior oblique (IO): In the primary eye position, the muscle plane of the IO makes an angle of 51° with the visual axis. The primary action of the muscle is extorsion, while the secondary actions are abduction and elevation (Figure 8).

Table 1: Actions of the extraocular muscles

ElevationExtorsionInferior obliqueIntorsionElevationSuperior rectus

DepressionIntorsionSuperior obliqueExtortionDepressionInferior rectus

Secondary ActionPrimary ActionMuscle

Right superior SD upregulation – the slow phase of nystagmus (Figure 10):♦Path 1: Right VN afferents → cross the midline and ascend in the left MLF →

IO subnucleus of left IIIrd nerve nucleus → left IIIrd nerve → left IO.♦Path 2: Right VN afferents → cross the midline and ascend in the left MLF →

SR subnucleus of left IIIrd nerve nucleus → cross the midline to the right IIIrdnerve → right SR.

♦The eyes move upward and clockwise (observer’s view).

Right superior SD upregulation – the fast phase of nystagmus (Figure 11):♦Path 1: Left riMLF → cross midline to the IR subnucleus of right IIIrd nerve

nucleus → right IIIrd nerve → right IR.♦Path 2: Left riMLF → cross the midline to the right IVth nerve nucleus → left

IVth nerve → left SO.♦Simultaneous contraction of these muscles causes a downbeating and

counterclockwise (observer’s view) motion.

Table 2: SD connections with the yoked eye muscles and their actions:

Fast phase downwards & counterclockwiseRight IR + Left SO

Slow phase upward & clockwiseRight SR + Left IO

Superior ampullofugal

Fast phase upwards & counterclockwiseRight IO + Left SR

Slow phase downwards & clockwiseRight SO + Left IR

Posterior ampullofugal

Fast phase to the rightRight LR + Left MR

Slow phase to the leftRight MR + Left LR Horizontal ampullopetal

ActionYoked MusclesRight SD

DiscussionReflexive VOR eye movements have a common final pathway from the IIIrd, IVth

and VIth nerve nuclei to their corresponding extraocular muscles. The connections between the vestibular nuclei and the oculomotor nuclei - and the motor nerves of these muscles - are unique in that they cause eye conjugate eye movements from unilateral stimulation. To achieve this, each SD has a major connection to one ipsilateral and one contralateral extraocular muscle. The conundrum of simultaneously stimulating two nerves on different sides of the body from a unilateral source is elegantly overcome by the arrangement shown in Figure 2.

The pathways and underlying mechanisms causing the fast phase of horizontal nystagmus are understood (Figure 3). The PPRF and PH are key participants in the generation of the fast phases of nystagmus2. The fast phases of vertical nystagmus are generated in the riMLF, but the trigger and pathways are not as clearly delineated as they are with the horizontal fast phases.

Conclusions♦Each SD has a major connection to one ipsilateral and one contralateral

extraocular muscle.♦Reflexive eye movements generated by the horizontal SDs result in a purely

horizontal motion.♦Reflexive eye movements generated by the vertical SDs are with either up or

down drift, and always with a torsional component.♦All the VN axons from each of the SDs cross the midline before synapsing with

their respective VIth, IIIrd, and IVth nerve nuclei.♦Conjugate eye movements are possible because the third and fourth order axons

recross the midline.♦Torsional eye movements follow vertical SD inputs because of the angle between

the visual axis and the orbital axis.♦The pathways and triggers for the fast phases of horizontal nystagmus are

known2.♦The pathways and triggers for the fast phases of vertical and torsional nystagmus

are only partially understood.♦The pre-motor neurons for torsional and downward fast phase eye movements

are located in the riMLF. The right riMLF triggers clockwise rotation, while the left one triggers counter-clockwise rotation5.

References1. Leigh RJ, Zee DS. The neurology of eye movements. Oxford: Oxford

University Press; 2006. p. 20-107.2. Markham CH. How does the brain generate horizontal nystagmus? In: Baloh

RW, Halmagyi GM, editors. Disorders of the vestibular system. New York: Oxford University Press; 1996. p. 48-61.

3. Dale RT. Fundamentals of ocular motility and strabismus. New York: Grune & Stratton; 1982. p. 1-28.

4. Nelson LB, Catalano RA. Anatomic relationships. In: Atlas of ocular motility. Philadelphia: W.B. Saunders; 1989. p. 2-37.

5. Horn AK. The reticular formation. Prog Brain Res 2005; 151:127-155.

Right posterior SD pathways (Figure 4):♦Path 1: Right VN afferents → left MLF → lR subnucleus of left IIIrd nerve

nucleus → left IIIrd nerve → left inferior rectus (IR).♦Path 2: Right VN afferents → left MLF → left IVth nerve nucleus → right

IVth nerve → right superior oblique (SO).

Right posterior SD upregulation – the slow phase of nystagmus:The left IR (depression and extortion) and the right SO (depression and intorsion) contract simultaneously, causing a conjugate downward driftand clockwise rotation (observer’s view) of the eyes (Figure 4).

Right posterior SD upregulation – the fast phase of nystagmus (Figure 9): Vertical pre-motor burst neurons, essential for generation of vertical and torsional saccades, have been identified in the pre-tectal region of the rostral interstitial nucleus of the MLF (riMLF)5.♦Path 1: Left riMLF → cross the midline to the SR subnucleus of the

right IIIrd nerve nucleus → left IIIrd nerve → left SR.♦Path 2: Left riMLF → cross the midline to the IO subnucleus of the right

IIIrd nerve nucleus → right IIIrd nerve → right IO.♦Simultaneous contraction of these muscles causes an upbeating and

counterclockwise (observer’s view) motion.