to develop, version testing often shows overaction of the antagonist inferior oblique muscle with little or no underaction of the paretic superior oblique muscle. Kushner313 has attributed the inferior oblique overaction associated with unilateral trochlear nerve palsy to a combination of strengthening and contracture. As the trochlear nerve palsy becomes chronic, spread of comitance develops, which leads to vertical measurements that are similar in abduction and adduction. Spread of comitance in long-standing trochlear nerve palsy can result from contracture of the superior rectus on the affected side (secondary to a chronic hyperdeviation) or from a contracture of the contralateral inferior rectus muscle (secondary to a contralateral hypotropia in a patient who habitually fixates with the paretic eye). In children who prefer fixation with the paretic eye, overaction of the antagonist inferior oblique muscle initially produces a “fixation duress” in gaze opposite the palsy, requiring excess downward innervation to fixate in horizontal gaze. This excess innervation may produce the appearance of a paretic superior rectus muscle on the contralateral side when versions are tested. When ductions are tested, however, movement of the eye in the field of action of the underacting superior rectus muscle is found to be normal.

The appearance of superior rectus paresis contralateral to a trochlear nerve palsy when the paretic eye is used for fixation has been termed inhibitional palsy of the contralateral antagonist.572 Over time, the fixation duress produced by fixation with the paretic eye results in an inferior rectus contracture in the opposite eye, causing hypotropia with restricted elevation, and sometimes enophthalmos (the fallen eye syndrome).143 Such patients may be mistakenly thought to have a blowout fracture or a double elevator palsy in the contralateral eye. However, neuroimaging shows atrophy or hypoplasia of the paretic superior oblique muscle. These patients present a confusing diagnostic picture because the inferior rectus contracture may cause a hyperdeviation that is greater in upgaze than downgaze. For reasons that are poorly understood, subjective and objective fundus torsion may be localized to the nonparetic eye (perhaps attributable in part to the inferior rectus contracture). Once the appropriate ductions and versions are measured and the three-step test performed, the correct paretic muscles can usually be identified. Patients with acquired trochlear nerve palsy who habitually fixate with the paretic eye often report subjective excyclotropia of the nonparetic eye.414 This phenomenon results from a sensory adaptation to the cyclodeviation by means of a reordering of the spatial response of retinal elements along new meridians.414

Three-Step Test

The three-step test is a diagnostic protocol originating from the work of Bielschowsky and popularized by Parks.426 The technique has several variations,217,228,232 but all address the

same three questions: (1) Is there a right or left hypertropia in primary position? (2) Does the deviation increase in right gaze or left gaze? (3) Does it increase with head tilt to the right or to the left? With this test, an isolated paretic cyclovertical muscle can be identified in most cases.

Analysis of the three-step test involves sequential elimination of possible weak muscles responsible for the vertical misalignment until only one choice remains. For example, a patient with a right hypertropia could have weakness of the depressors of the right eye (right inferior rectus or superior oblique muscles) or the elevators of the left eye (left superior rectus or inferior oblique muscles). If the deviation is greater in left gaze and less in right gaze, then the right superior oblique and left superior rectus muscles are the possible paretic muscles because these muscles are responsible for depressing the right eye in left gaze and elevating the left eye in left gaze. If, on head tilt testing, the deviation increases in right head tilt and decreases in left tilt, then the right superior oblique is implicated since the right superior oblique and superior rectus muscles work in concert to incycloduct the right eye during right head tilting. The depression and elevation action of these two muscles is normally offsetting, maintaining the vertical position of the eye. When the superior oblique is weak, the elevating action of the superior rectus muscle is unopposed, and the eye further elevates when the incycloduction is stimulated by right head tilting. The left superior rectus muscle is not innervated in excycloduction of the left eye (the torsional movement stimulated by right head tilt) and, therefore, is eliminated from consideration in the situation of increased vertical deviation during right head tilting. On the basis of the work of Wong and Sharpe602 Gamio has proposed that some patients with paretic strabismus can show changes in horizontal alignment with head tilt to either side.182

The general mechanism that underlies the Bielschowsky Head Tilt test, first proposed by Nagel394 in 1871, and later by Hofmann and Bielschowsky233 in 1900, is still generally accepted.489,577 Reports of central vestibular dysfunction as a putative cause of head tilt514 probably represent patients with skew deviations and ocular tilt reactions who were thought to have unilateral trochlear nerve palsy. However, Wong et al have demonstrated both deficits and compensatory adaptations in the vestibulo-ocular reflex in patients with trochlear nerve palsy.603

Kolling et al292 investigated the effects of Marlow occlusion in patients with unilateral trochlear nerve palsy. They found a shift to horizontal incomitance in their group who started out with horizontally-comitant deviations but little change after prolonged occlusion of the involved eye in their group of 18 patients who started with horizontally incomitant hyperdeviations. They concluded that Marlow occlusion may be necessary to uncover the real vertical deviations that characterize unilateral trochlear nerve palsy and that the post-occlusion pattern of hyperdeviation in different fields of gaze should be used to direct surgical management.

A positive three-step test does not necessarily implicate an isolated vertical muscle palsy as the causative factor. Kushner309 reviewed a group of patients with positive threestep tests who had multiple muscle paresis, dissociated vertical deviation, previous vertical muscle surgery, skew deviation, myasthenia gravis, and small nonparalytic vertical deviations associated with horizontal strabismus. He cautioned that the results of the three-step test must be interpreted in the context of the clinical history and associated neuro-ophthalmologic findings.

Absence of tone in the superior oblique muscle, allows an eye to rotate into an extorted position. Because the amount of torsion in unilateral trochlear nerve palsy (about 5°) falls within a child’s sensory cyclofusional range, most (77%) of the patients with acquired trochlear nerve palsy do not complain of image tilt under normal seeing conditions.576 Furthermore, such children can fuse when a vertical prism is placed before one eye to neutralize the deviation. Subjective torsion is usually measured with the Double Maddox Rod test. Objective torsion is generally evaluated by observing the horizontal position of the optic disc relative to the macula, using indirect ophthalmoscopy (in the absence of torsion, the macula should be aligned horizontally with the lower third of the optic disc). In addition to isolated oblique muscle paresis, objective torsion may also be seen in children with primary oblique muscle overaction. The commonly used term “macular torsion” is incorrect, because rotation of the globe in primary gaze occurs around a sagittal axis that goes through the macula. Confirmation of objective torsion is especially important in preverbal children.56 Patients with trochlear nerve palsy show persistent extorsion in the paretic eye on head tilt to either side,209,314 indicating that the compensatory head tilt serves to neutralize the vertical and not the torsional deviation.314

Discrepancies between subjective and objective tests are common in children with congenital superior oblique palsies (who may deny subjective torsion despite objective torsion)206,415 and in children who habitually fixate with the paretic eye (who may have objective torsion in the fixating eye but subjective torsion in the opposite eye).415

Although most unilateral superior oblique palsies are isolated lesions, a careful search should be made for localizing signs.66 For example, a lesion that affects the dorsal midbrain might cause upward gaze palsy and other signs of dorsal midbrain syndrome.66 An intramedullary lesion involving the fascicular portion of the fourth nerve may also involve the descending sympathetic tract to produce a contralateral Horner syndrome or the medial longitudinal fasciculus to produce an internuclear ophthalmoplegia.66,270 A lesion that affects the trochlear nucleus or fascicle (most commonly a trochlear nerve schwannoma) or the adjacent brachium of the superior colliculus produces a trochlear nerve palsy with a contralateral afferent pupillary defect but no associated visual field defect.156 Associated ocular motor nerve palsies suggest an intracavernous or orbital apical lesion. Kushner has noted that the results

of Bielschowsky Head Tilt testing in trochlear nerve palsy cannot be explained simply by the classic model of altered otolithic input to the four vertical rectus muscles. For example, the Bielschowsky Head Tilt test difference typically decreases in patients with unilateral superior oblique muscle palsy after inferior oblique muscle weakening. Also, inferior oblique overaction increases gradually over months to years, and the size of the Bielschowsky Head Tilt test difference gradually increases.197 Gräf et al197 speculated that there may be an adaptive mechanism that causes the size of the head tilt to gradually increase over time by amplification of the otolith reflex in response to vertical fusional vergence.412 Eye movement recordings during dynamic tilt, show a circular rotational trajectory in the affected eye, corresponding to a nasal deviation of the rotation axis toward the line of sight.588 In long-lasting trochlear nerve palsy, the extorsion decreases while the hypertropia and head tilt phenomenon increase,291 possibly reflecting a superimposed ipsilateral superior rectus contracture. Kommerell and Klein294 proposed that gain modulation of the otolith reflex could be caused by the chronic head tilt.

Trochlear nerve palsy leads to kinematic aberrations of both the paretic and the unaffected eye. During dynamic head roll, the rotation axis of the covered paretic or unaffected eye deviates inward, while the rotation axis of the viewing paretic or unaffected eye aligns with the line of sight.588 During downward saccades, the trajectories of both eyes curve towards the unaffected side529; these curvatures increase when the head is rolled to the affected side and the gaze directed to the unaffected side.533 Hence, during both vestibular evoked and saccadic ocular movements, the unaffected eye shows similar kinematic aberrations as the paretic eye. While aberrations of the paretic eye can be explained by decreased force of the superior oblique muscle, aberrations of the unaffected eye may be due to increased force parallel to the paretic superior oblique muscle in the unaffected eye, in accordance with Hering’s law.

Three-dimensional eye positions expressed as rotation vectors normally lie in a plane, called Listing’s plane. Listing’s plane in eyes with acquired trochlear nerve palsy is rotated temporally, which reflects the fact that vertical eye movements are associated with true torsion (up-extorsion, down-intorsion).534 The orientation of Listing’s plane in the presence of “congenital trochlear nerve palsy,” however, is not different from normal eyes. Hence, similar to anatomical studies, kinematical analyses of 3D eye positions suggest that congenital trochlear nerve palsy eventuates in a different set of ocular rotations.

Bilateral Trochlear Nerve Palsy

The incidence of bilateral paresis in a series of trochlear nerve palsies has been estimated at 8%.301,308 While most cases are traumatic in origin, bilateral trochlear nerve palsy