Functional imaging of human extraocular muscles in head tilt dependent hypertropia

Abstract

Purpose: Although alteration in hypertropia induced by head tilt is considered a clinical criterion for diagnosis of superior oblique (SO) palsy, the mechanism of this head-tilt-dependent hypertropia (HTDHT) is unclear. In this study, magnetic resonance imaging (MRI) was used to study extraocular muscle (EOM) responses to head tilt in HTDHT.

Methods: Orbital MRI was used to study 16 normal subjects and 22 subjects with HTDT, of whom 12 had unilateral SO atrophy and 10 had "masquerading" SO palsy with normal SO size. Sizes and paths of all EOMs were compared in 90° roll tilts.

Results: Normal subjects exhibited the expected 3° to 7° physiologic extorsion of all four rectus pulleys in the orbit up-versus-down roll positions, corresponding to ocular counterrolling. In orbits with SO atrophy, the lateral (LR) and inferior rectus (IR) pulleys paradoxically intorted by approximately 2°. Subjects with HTDHT but normal SO size exhibited reduced or reversed extorsion of the medial, superior, and LR pulleys, whereas pulley shift was normal in nonhypertropic fellow orbits in HTDHT. In normal subjects and in SO atrophy, the inferior oblique (IO) muscle contracted in the orbit up-versus-down roll position, but paradoxically relaxed in HTDHT without SO atrophy.

Conclusions: The ipsilesional IR and LR pulleys shift abnormally during head tilt in HTDHT with SO atrophy. In HTDHT without SO atrophy, the ipsilesional MR, SO, and LR pulleys shift abnormally, and the IO relaxes paradoxically during head tilt. These widespread alterations in EOM pulling directions suggest that complex neural adjustments to the otolith-ocular reflexes mediate HTDHT.

Figure 1.

Quasi-coronal T2FSE MRI in planes close to the rectus pulleys, in a subject with left SO palsy. Blue insets: are axial views indicating actual head orientation relative to gravity: top panels tilted right down and bottom panels tilted left down. The right orbit appears on the left. Green lines connect corresponding horizontal and vertical rectus pulleys in the normal right orbit, and show with green arrows normal pulley array rotation counter to head tilt. If it had been normal, the left orbit would have shown clockwise rotation with the same sense as the left orbit in right down and counterclockwise with the left down. Instead, magenta lines in the left orbit with SO palsy show reduction of the pulley array rotation. IR, inferior rectus muscle; LPS, levator palpebrae superioris muscle; LR, lateral rectus muscle; MR, medial rectus muscle.

Figure 2.

Quasi-sagittal MRI in plane of the inferior rectus (IR) center, in subject with left SO palsy depicted in Figure 1. Note that for both inferior oblique (IO) muscles, the cross section (white dotted outlines) is larger in the upper than in the lower orbit during 90° roll tilt. ON, optic nerve.

Figure 3.

Quasi-coronal MRI in midorbit of the subject with left SO palsy illustrated in Figures 1 and 2. The cross section of the normal right SO is larger than that of the palsied left SO in central gaze, and the cross section of the right but not the left SO increases from up to down gaze. This represents neurogenic atrophy of the left SO. Abbreviations as in Figures 1 and 2.

Figure 4.

The effect of 90° upward and downward roll tilt on coronal plane coordinates of the four rectus pulleys, referenced to the globe center, in 31 normal control orbits and 12 affected and 12 fellow orbits in subjects with SO palsy. Error bars, 95% confidence intervals. Solid and broken lines between coordinates in the center panel connect the normal pulley array. The four side panels expand data for individual pulleys. Note the torsional shifts of normal rectus pulleys (center graph), but the complex pattern of different shifts in palsied and fellow orbits in SO palsy.

Figure 5.

Torsional shift of rectus pulleys in the 90° roll tilt up-versus-down positions in 31 normal control orbits and 12 affected and 12 fellow orbits in subjects with SO palsy and in 10 hypertropic and 10 hypotropic orbits of subjects with masquerading SO palsy. Note the reversed shift of LR and IR pulleys in the orbits with SO palsy, but different patterns of pulley shift in both orbits in masquerading SO palsy. Deg, degrees; Hyper, hypertropic; Hypo, hypotropic.

Figure 6.

Maximum SO cross section, averaged for right and left head tilts. The SO cross section was highly significantly reduced from normal in the hypertropic orbit in SO palsy, but increased from normal in the hypertropic orbit in masquerading SO palsy. SO cross sections in hypotropic orbits of both SO true and masquerading palsies did not differ from normal. Error bars, SEM.

Figure 7.

Inferior oblique (IO) cross section in the image plane of the IR crossing. (A) There was no significant variation from normal in mean cross-sectional area in the orbit of subjects with either true or masquerading SO palsy. (B) Normal subjects exhibited significantly larger IO cross section in tilt-up minus tilt-down position, as appropriate to extorsional ocular counterrolling. IO muscles in hypertropic orbits of subjects with masquerading palsy, but no other orbits, exhibited significant reduction in IO cross section in tilt-up minus tilt-down positions, interpreted as paradoxical IO relaxation.