Major ReviewSkew Deviation Revisited
Introduction
According to Stedman's Medical Dictionary,184 skew deviation refers to “a hypertropia in which the eyes move in opposite directions equally; an acquired hypertropia, often fairly comitant, not fitting the characteristic pattern of trochlear nerve damage or of ocular muscle abnormality; often due to a brainstem or cerebellar lesion.” For many years, skew deviation was held to be a nonlocalizing sign and a diagnosis of exclusion.84, 112 Skew deviation usually presents as a comitant hypertropia in a patient with posterior fossa disease.44 In rare cases, however, it can increase in one horizontal direction of gaze, manifest as a paroxysmal hyperdeviation of one eye, or produce alternating hyperdeviations in gaze to either side.44, 181 The purpose of this review is to acquaint the reader with advances in our understanding of skew deviation as a clinical diagnostic entity, in terms of its clinical range of presentation, its underlying pathophysiology, and its clinical localizing value.
Section snippets
History
Skew deviation was first recognized experimentally in animals by the experimental physiologist Francois Magendie in 1824.131 The following year, Henry Hertwig described skew deviation in a cat following an incision through the cerebellum into the medulla.100, 182 In 1904, Stewart and Holmes observed skew deviation in a man with a cerebellar tumor, and in other patients following craniotomies for cerebellar tumors.186 During World War I, Gordon Holmes documented skew deviation in 5 of 40
Causes
Skew deviation can result from any acute injury within the posterior fossa (ischemic infarction, multiple sclerosis, tumor, trauma, abscess, hemorrhage, syringobulbia, or neurosurgical procedures).12, 44, 116, 181 The majority of cases are seen in association with brainstem stroke.61, 181 A lesion need not involve the brainstem or cerebellum to cause skew deviation, however. Acute unilateral vestibular lesions can also cause skew deviation.61, 63, 90, 91, 113, 116, 167, 219
Numerous rarer causes
Evolutionary Underpinnings
Classical skew deviation occurs in the context of an ocular tilt reaction, in which bilateral otolithic input is leveraged by the central vestibular system to modulate extraocular muscle and postural tonus in the roll plane (the plane in which the head or body tilts from side to side).136, 176, 223 The ocular tilt reaction in humans is probably a vestigial remnant of the primitive otolithic righting reflex that is released only under pathological conditions.136 The relative preponderance of the
Neuroanatomy
The primary functions of the vestibulo-ocular system are to maintain eye position and stabilize fixation during head movements. The labyrinthine receptors transduce the forces associated with head acceleration into a biological signal.136 The semicircular canals sense angular acceleration, while the otoliths (the saccules and utricles) respond to linear acceleration (i.e., head translation and the most pervasive form of linear acceleration, the pull of gravity).136 In lateral-eyed animals and
Symptomatology
Unilateral lesions or stimulation of the utricles or vertical semicircular canal pathways cause an imbalance of vestibular tone in the roll plane, which results either in a complete (tonic or paroxysmal) ocular tilt reaction or in single components of the ocular tilt reaction such as cyclorotation of the eyes or skew deviation.64
In the pathological ocular tilt reaction, the eyes, head, and body are continuously adjusted to what the central nervous system erroneously computes as being vertical.29
Subjective Visual Tilt
The ocular tilt reaction is associated with a tilt in the subjective visual vertical. This term is often confusing to the uninitiated reader because the patient remains asymptomatic, and even when asked, states that his or her surroundings do not appear tilted. However, the patient's subjective visual world (which he or she perceives as upright) is indeed tilted with respect to the true earth vertical. In this sense, the patient can be said to experience a subjective visual tilt. It is as if
Localizing Value
To ascertain the localizing value of skew deviation, Brandt and Dieterich reviewed 155 patients with the clinical diagnosis of acute unilateral brainstem infarction.26 Fifty-six (36%) of these patients demonstrated skew deviation. Skew deviation was always associated with ocular torsion, which affected both eyes in 50%, the lowermost eye in 31%, and the uppermost eye in 19%. The direction of the ocular torsion inevitably corresponded to the direction of skew (i.e., intorsion of the right eye
Sites of Injury
The ocular tilt reaction indicates a unilateral peripheral deficit of otolithic input or a unilateral lesion of graviceptive brainstem pathways from the vestibular nucleus (crossing midline at the pontine level) to the interstitial nucleus of Cajal in the rostral midbrain.25 The resultant head tilt, torsion of the eyes, skew deviation, and tilt of the subjective visual vertical are the postural, ocular motor, and perceptual manifestations of a single lesion of those vestibular pathways
Clinical Subtypes
Smith et al divided skew deviation into three classic subtypes (comitant, laterally comitant, and lateral alternating skew deviation).181 Additional forms such as paroxysmal skew deviation, alternating skew deviation, and transient neonatal skew have since been recognized.
General
Skew deviation and its associated ocular tilt reaction are usually readily differentiated from the vertical ocular misalignment caused by restriction (blow out fracture, congenital fibrosis syndrome, Brown syndrome, orbital fibrous bands, paretic disease—some forms of double elevator palsy, superior or inferior division third nerve palsy, etc.), neuromuscular junction disease (myasthenia gravis), innervational disorders (dissociated vertical divergence), and rare disorders such as extraocular
Expanding the Definition of Skew Deviation
Our traditional application of the term skew deviation to patients with neurologic disease leaves us with a hemianopic view of this disorder and its underlying physiology. In lower animals, the central vestibular system uses weighted graviceptive input from the two labyrinths and weighted visual input from the two eyes to establish subjective vertical orientation in the roll and pitch plane.38 These primitive reflexes can be detected in normal humans, wherein a cycloversion movement (a
Prognosis and Treatment
Because most ocular tilt reactions are transient and spontaneous recovery is the rule,18, 123 surgical therapy should be deferred for several months. During this period, prismatic treatment or botulinum therapy can provide adequate symptomatic relief of vertical diplopia. Prisms, botulinum toxin, and vertical rectus muscle recession have all been touted as effective treatments for vertical diplopia secondary to persistent skew deviation.40, 123, 146, 160, 174 The resolution of the ocular tilt
Questions
Our enormous progress in elucidating the pathophysiology of skew deviation raises a number of new questions. Because skew deviation is often associated with conjugate ocular torsion, are some patients with unilateral otolithic dysfunction using a combination of horizontal and vertical convergence to fuse a hyperphoria? Perhaps patients with manifest hypertropia represent the most severe end of the spectrum. Is the subjective visual tilt necessarily the cause of the skew deviation, ocular
Conclusions
Skew deviation has evolved from a descriptive term to a precise physiological mechanism of injury. Skew deviation results from a unilateral lesion that unilaterally injures the otolithic pathways and thereby causes the brain to perceive the world as tilted. The resulting vertical deviation is but one part of an ocular tilt reaction which rotates the eyes and head toward the tilted visual world to restore vertical orientation. Skew deviation can be caused by a lesion to utricular pathways
Method of Literature Search
References were obtained from English and non-English references for skew deviation, and ocular tilt reaction. English references from 1966 to 2005 were obtained from MEDLINE, and older English and non-English references were obtained from neuro-ophthalmology textbooks and major articles that addressed the topic of skew deviation. Due to the large number of experimental animal studies investigating the ocular motor consequences of brainstem or cerebellar lesioning on vertical ocular alignment,
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Supported in part by a grant from The Pat and Willard Walker Foundation, Jones Eye Institute, and Research to Prevent Blindness, Inc. The authors reported no proprietary or commercial interest in any product mentioned or concept discussed in this article.