Head Tilts

Incomitant Strabismus

Any vertical extraocular muscle paresis may necessitate a compensatory head tilt to achieve binocular vision.34 Isolated vertical muscle weakness resulting from disease involving the neuromuscular junction or the muscle itself can lead to similar findings. Head tilting is often the salient clinical feature of an isolated oblique muscle palsy, whereas a head tilt that occurs in conjunction with an abnormal vertical head position often signifies an isolated vertical rectus muscle palsy. Most studies have found superior oblique palsy to be the most common single cause of a head tilt.134,162,168,202,211

The long intracranial course of the fourth cranial nerve, which innervates the superior oblique muscle, renders it particularly susceptible to injury from head trauma. Unilateral superior oblique paresis produces excyclodeviation and a hyperdeviation of the involved eye. Patients with uncomplicated unilateral superior oblique palsy tilt their heads contralateral to the side of the injured nerve to restore single binocular vision. This compensatory head posture causes the otolith apparatus to increase innervation to the extorters (inferior oblique muscle and inferior rectus muscle) of the involved eye and decrease innervation to the intorters (superior rectus muscle and superior oblique muscle), thus minimizing the mechanical advantage of the superior rectus muscle (an elevator) over the paretic superior oblique muscle (a depressor). However, tilting the head ipsilaterally to the side of the injured nerve causes the otolith apparatus to stimulate the intorters (the superior rectus muscle and superior oblique muscle) and inhibit the extorters (the inferior rectus muscle and inferior oblique muscle) of the involved eye, which provides a mechanical advantage to the superior rectus muscle over the paretic superior oblique muscle, resulting in worsening of the hyperdeviation.135

Because the head tilt recruits physiologic otolithic innervation to compensate for vertical misalignment of the eyes, and because supine positioning eliminates otolithic input, parents report that the head tilt is absent when the child lies down or sleeps. Because the hyperdeviation increases in adduction, children with superior oblique palsy often have a head turn in the direction of the tilt to position the paretic eye in abduction.162 In rare cases, the head turn can predominate.

The patient with superior oblique palsy tilts his/her head to eliminate the vertical deviation rather than the torsional deviation, which can be overcome by adaptive mechanisms, including sensory cyclofusion, as well as other psychologi- cal-experiential and physiological-sensory adaptations.99,206 (Placing a prism in front of either eye of a patient with superior oblique palsy to match the vertical deviation eliminates

the vertical deviation and causes the head tilt to resolve, despite persistence of the monocular extorsion.)206

Occasionally, children with superior oblique palsy seem unable to adapt to a monocular cyclotropia, in which case the cyclotropia (without an accompanying vertical deviation) can be the exclusive source of the torticollis.206 Children whose head tilt disappears on covering the paretic eye and persists when the nonparetic eye is covered probably fall into this group. Because binocular vision is disrupted when either eye is covered and symptoms of hypertropia are thus eliminated, only cyclotropia could explain the persistence of the head tilt when the sound eye is covered.206 Under binocular conditions, such a child would assume a compensatory head tilt to the opposite shoulder when the involved eye fixates and would have no compensatory head posture when the uninvolved eye fixates.131,205,206 These children may have difficulty adapting to acquired monocular torsion in a dominant eye. Alternatively, the observation that monocular extorsion produces a stereoscopic tilt of binocular visual world toward the extorted eye23 makes it is possible that some of these children may be adapting their head positions to their tilted sense of visual vertical.

Some children with superior oblique palsy maintain a contralateral head tilt even though a manifest vertical strabismus exists and fusion is absent in the preferred head position.206 It has been speculated that, in such children, a long-standing head tilt may persist on a habitual basis; it may be secondary to unilateral contracture of the neck muscles, or it may serve to provide anomalous fusion on the basis of anomalous retinal correspondence.206 It is more likely, however, that these children have either DVD or the ocular tilt reaction that was misdiagnosed as superior oblique palsy.

It is said that a child with superior oblique palsy rarely tilts the head toward the side of the hypertropic eye (reportedly to maximize separation of diplopic images).131,206 However, the finding of a paradoxical head tilt should again lead one to consider the possibility of DVD, which can be associated with a head tilt toward or away from the side of the hypertropic eye.48 Reversal of a head tilt following surgery for superior oblique palsy may indicate a masked bilateral superior oblique palsy or a simple surgical overcorrection of the hyperdeviation (which produces a reversal of the Bielschowsky Head Tilt test that is indistinguishable from masked bilateral superior oblique palsy).186

Congenital and acquired superior oblique palsies differ with respect to their clinical manifestations and their underlying etiologies. In acquired palsies, the head position is marked, a noncomitant deviation is present, intermittent diplopia is common, and there is no facial asymmetry, except in longstanding deviations.207 In contrast, congenital superior oblique palsy is often associated with milder torticollis that has persisted since infancy (evident in old photographs),163 together with facial asymmetry (see Chap. 6).212 Contrary to the prevailing

dogma that children with superior oblique palsy do not have sufficient head control until 6 months of age to maintain a compensatory head tilt for fusion, we have seen an infant who showed a head and body tilt starting in the first month of life.29 In the absence of head control, this infant allowed gravity to passively tilt her head and body in the compensatory direction to optimize utricular input for vertical fusion. At 6 months of age, her motor control enabled her to maintain a head tilt while maintaining her trunk in the neutral position. Thus, the onset of a unidirectional head tilt within the first few months of life should not be considered diagnostic of congenital muscular torticollis.

Large vertical fusional vergence amplitudes are also highly characteristic of congenital or long-standing superior oblique palsy.207 In contradistinction to congenital muscular torticollis, the head tilt associated with congenital superior oblique palsy resolves in the supine position, usually resolves with monocular patching, and exhibits no limitation to passive rotation in the opposite direction.207 Recognition of these features is crucial in establishing the diagnosis of congenital fourth nerve palsy, because spread of comitance may develop over many years, obscuring the characteristic ocular motility pattern. Many patients with congenital superior oblique palsy and torticollis deny diplopia, but some present with acute vertical diplopia when they lose control of their deviation. Unlike patients who acquire superior oblique palsy from an injury to the trochlear nerve, many patients with congenital superior oblique palsy are found at surgery to have lax, misdirected, or absent superior oblique tendons.172 It is unclear whether such cases of congenital superior oblique palsy result from congenitally absent trochlear innervation or a primary dysgenesis of the superior oblique muscle. Polymorphisms in this homeo- box-containing ARIX gene may be responsible for some cases of congenital superior oblique palsy.121

A head tilt or turn can produce facial asymmetry, with an appearance of facial compression or reduced facial mass, ipsilateral to the tilt or turn in torticollis from a wide variety of causes.94 Because a head tilt or turn from any cause can eventuate in facial asymmetry (termed deformational plagiocephaly), this facial asymmetry in undiagnosed torticollis cannot be used to suggest an ocular cause. Bone, muscle, fat, and skin are all living tissues that undergo continuous turnover and remodeling throughout life (similar to the increasing arm length of tennis players on the side of the stroke arm).132 Gravity may also play a role in the tilt of the tip of the nose toward the side of the head tilt (pointing directly to the ground in the preferred head position). The complete facial asymmetries are three dimensional, requiring several different views to fully appreciate.94 Greenberg and Pollard94 found that the nasal tip tends to point toward a head tilt, but away from a turn.212 In superior oblique palsy, the head tilt and turn are commonly in the same direction, producing opposing forces in directing the nasal tip deviation. Thus, in

patients with superior oblique palsy who have nasal tip deviation away from the torticollis, the head turn may be more causally significant than the tilt.

Although deformational plagiocephaly has been attributed to abnormal sleep positioning,88 disappearance of the head tilt in the supine position belies this hypothesis.170 It has been reported that visual field deficits can be associated with deformational plagiocephaly, although neither the laterality nor the severity of skull deformity is predictive of these visual field defects.189

Synostotic Plagiocephaly

Patients with synostotic plagiocephaly have premature fusion of the coronal suture on one side of the skull.8,65 This cranial abnormality leads to ipsilateral forehead and orbital retrusion, contralateral forehead protrusion, orbital and lateral canthal dystopia, and contralateral zygomatic and occipital flattening65 (Fig. 9.2). Affected infants manifest unilateral superior oblique dysfunction and tilt their head contralateral to the side of the retruded orbit.8,65,80 In synostotic plagiocephaly, wherein malpositioning of the trochlea associated with an osseous (i.e., musculoskeletal) abnormality leads to superior oblique tendon laxity and signs and symptoms of superior oblique palsy. Weakness of the superior oblique muscle results from a desagittalization and laxity of the superior oblique tendon within the retruded orbit (Fig. 9.3), as well as excyclorotation of the extraocular muscles. The secondary form of plagiocephaly (deformational) results from the asymmetrical effects of congenital muscular torticollis on craniofacial growth. Thus, unlike deformational plagiocephaly, which can gradually result from congenital superior oblique palsy, synostotic plagiocephaly can be the cause of the palsy.80

Fig. 9.2  Infant with right synostotic plagiocephaly. Note retrusion of right forehead and orbit, elevated right superior orbital rim, widened right palpebral fissure, left forehead protrusion, and head tilt to left

Fig. 9.3  Relationship between inferior oblique muscle and superior oblique tendon in synostotic plagiocephaly. View from below depicts right orbit on left-hand side of page. Desagittalization of superior oblique tendon occurs due to retruded right orbit and right trochlea relative to inferior orbital rim

Spasmus Nutans

Nystagmus accompanied by head oscillations and torticollis in an infant or young child is highly suggestive of spasmus nutans. In 1906, Still193 rhapsodically summarized the sensation of observing a child with spasmus nutans:

“Hardly less striking than this rhythmic unsteadiness of the head is the curious way the child has of looking at objects out of the corner of his eyes with the head slightly averted and the face turned slightly downwards, reminding one of the behavior of the Beaver in The Hunting of the Snark, for as you may remember,

‘Whenever the butcher was by,

The Beaver kept looking the opposite way And appeared unaccountably shy.’

The other feature which attracts attention is the exceedingly fine rapid nystagmus which is peculiar in being so much more marked in one eye than the other, that it may appear to be actually limited to one eye, a point which the mother herself has usually noticed.”

The appearance of the nystagmus alone in spasmus nutans is fairly distinct, in that it resembles an ocular shiver that may be so fine and rapid as to be barely visible.91 It may be horizontal, vertical, or torsional in direction.107 The clinical appearance of spasmus nutans differs from that of infantile nystagmus in that spasmus nutans is often asymmetrical and may actually be monocular. It also differs in its usual time of onset (4 months to a year in spasmus nutans versus 2 or 3 months of age in congenital nystagmus).45 Although usually a benign, self-limited entity, MR imaging is warranted in children with spasmus nutans, because children with congenital suprasellar tumors may present with an identical constellation of findings.90,159 Neurodegenerative disorders188 and congenital retinal dystrophies may also rarely masquerade as spasmus nutans.

The high-frequency nystagmus that characterizes achromatopsia resembles that of spasmus nutans but is conjugate rather than asymmetrical.92

The compensatory nature of the head oscillations in spasmus nutans is discussed below. While the cause of the associated torticollis remains speculative, Gottlob et al91 believe that it may serve to directionalize the visually compensatory head nodding to its optimal trajectory.

Infantile Nystagmus

Children with infantile nystagmus occasionally utilize a head tilt to damp their nystagmus. In this setting, a careful search for an underlying cyclovertical muscle palsy should be undertaken before attributing the head tilt to a torsional null position. Infantile nystagmus with a torsional null position should increase in intensity when the patient’s head is straightened or tilted to the opposite side.

Strabismus surgery is remarkably effective in treating head tilts in patients with infantile nystagmus.58,191,208 These procedures involve transposing the horizontal, vertical, or oblique muscles to rotate the eyes in the direction of the head tilt to produce a contradirectional tilt of the visual world that drives the patient to tilt the head back toward vertical to realign it with the perceived visual world. However, it has not been established whether this procedure works by correcting a pre-existing visual tilt (which could determine the null position of the nystagmus) or by creating a new tilt of the subjective visual vertical (akin to an ocular tilt reaction) that must be compensated. The fact that patients rarely complain of subjective tilt after this procedure argues in favor of the former possibility.

We examined one infant with oculocutaneous albinism, who would tilt her head 90 degrees when viewing a horizontally rotating optokinetic drum, then rotate her head in lockstep with any rotation of the spinning drum. This adaptation presumably allowed her to optimize vision by using her intact vertical optokinetic system.

Benign Paroxysmal Torticollis of Infancy

In 1969, Snyder190 described 12 infants with paroxysmal head tilts that lasted from 10 min to 2 days. In some infants, the torticollis was accompanied with vomiting, pallor, and agitation. When the torticollis resolved, the infants appeared normal until the next attack. After a period of months to years, the attacks subsided. Subsequent reports have shown a female predominance and a tendency for the attacks to occur upon awakening.

Paroxysmal torticollis of infancy is considered to be a migraine equivalent that primarily affects the vestibular system.167 It is characterized by recurrent episodes of head tilt secondary to cervical dystonia. Attacks are often accompanied by vomiting, pallor, and ataxia, settling spontaneously within hours or days. Episodes begin within the first 12 months of life and resolve by 5 years.82 Older children may complain of headache or vertigo during the attack. Later in life, some children develop benign paroxysmal vertigo, which may be a migraine variant. Affected children often have a strong family history of migraine headache. An infant with an episodic torticollis, complete interval recovery, a suggestive past history, and a family history of migraines need not be subjected to invasive and expensive diagnostic studies. Benign paroxysmal torticollis of infancy has been linked to the CACNA1A mutation, which is thought to affect cerebellar output.82

Dissociated Vertical Divergence

DVD is a common cause of head tilt in children.26 DVD occurs in the setting of infantile strabismus and is characterized by hyperdeviation of either eye when it is mechanically occluded or cortically suppressed.20 The head tilt that accompanies DVD illustrates the role of visuo-vestibular input into postural orientation. Just as the labyrinths are balance organs that calibrate graviceptive input to maintain vertical orientation, the two eyes are balance organs that modulate visual luminance input.27 Bilateral labyrinthine and visual input are yoked together in the central vestibular system to establish ocular and postural orientation.27

DVD corresponds to the dorsal light reflex in lower, lateral-eyed animals.20 In nature, vertical orientation is associated with equal luminance input from the sky to the two laterally placed eyes. When an overhead light is shined down from one side of a goldfish, the fish therefore tilts toward the light because unequal luminance input to the two laterally placed eyes evokes a tilt toward the light (Fig. 9.4).93,204 In the vertically stabilized fish, shining a light from one side elicits a compensatory vertical divergence of the eyes (that strives to realign the interpupillary axis with reference to the perceived vertical).93

When cortical binocular vision fails to develop in infancy, an atavistic resurgence of the dorsal light reflex manifests as DVD.20 It is, therefore, not surprising that some patients with uncorrected infantile esotropia, and others with DVD, maintain a head tilt toward the preferred eye (Fig. 9.4).54,139 This head tilt, which corresponds to the dorsal light reflex in fish, is not compensatory for binocular vision (as evidenced by the fact that it persists despite manifest vertical misalignment).54,139 As such, strabismus surgery to restore vertical

Fig. 9.4  Clinical algorithm for the differential diagnosis of DVDassociated head tilts. Used with permission from Brodsky et al26

alignment does not improve this head tilt, but torsional surgery can be used to alter the tilted subjective visual vertical and thereby eliminate the head tilt.

Some patients with DVD maintain a head tilt toward the side of the hyperdeviating eye. This head tilt is compensatory for binocular vision, because it recruits otolithic innervation to neutralize the oblique muscle innervation that causes DVD.20,21,26 For example, DVD with hyperdeviation of the left eye results from simultaneous innervation to the right superior oblique muscles and inferior oblique muscles.100 A head tilt to the right activates otolithic innervation to the right superior oblique and left inferior oblique muscles and thereby increases the left hyperdeviation. A head tilt to the left recruits otolithic innervation to neutralize this cyclovertical divergence (Fig. 11).21,26,162 Thus, a head tilt to the side of the hyperdeviating eye can serve as a compensatory means of recruiting otolithic innervation to control a hyperdeviation (Fig. 11). This recruitment of otolithic innervation explains Jampolsky’s observation that a normal Bielschowsky Head Tilt Test response in DVD is characterized by a hyperdeviation of either eye that increases or becomes manifest when the head is tilted to the opposite side.115 In this setting, strabismus surgery to restore vertical alignment eliminates the associated head tilt.184

In DVD, a superior rectus contracture can also develop in a chronically hyperdeviating eye, causing a compensatory head tilt toward the side of the fixing eye.116 In this setting, superior rectus recession can eliminate the head tilt (as predicted by preoperative prism placement). Various mechanisms by which DVD are known to be associated with a head tilt are summarized in Fig. 12.26

The neutral head position maintained by most patients with DVD may therefore represent a compromise position between two opposing drives.26 On the one hand, a head tilt toward the side of the fixing eye that is necessary to reestablish vertical orientation increases the hyperdeviation of the contralateral eye. On the other hand, a head tilt toward the side of the hyperdeviating eye that is necessary to minimize