CLINICAL SCIENCES Primary Oblique Muscle Overaction The Brain Throws a Wild Pitch Michael C. Brodsky, MD; Sean P. Donahue, MD, PhD Background: Sensorimotor and orbital anatomical inferior oblique overaction, which corresponds to a for- mechanisms have been invoked to explain primary ob- ward pitch in lateral-eyed animals, may result from vi- lique muscle overaction. sual disinhibition of central vestibular pathways to the extraocular muscle subnuclei that modulate upward ex- Methods: Review of primitive visuo-vestibular re- traocular muscle tonus. flexes and neuroanatomical pathways corresponding to vestibulo-ocular reflexes, and correlation with known Conclusions: Primary oblique muscle overaction reca- clinical abnormalities in patients with primary oblique pitulates the torsional eye movements that occur in lateral- muscle overaction. eyed animals during body movements or directional lu- minance shifts in the pitch plane. These primitive ocular Results: Bilateral superior oblique muscle overaction, motor reflexes become manifest in humans when early- which corresponds to a backward pitch in lateral-eyed onset strabismus or structural lesions within the poste- animals, can occur when structural lesions involving the rior fossa alter central vestibular tone in the pitch plane. brainstem or cerebellum increase central otolithic input to the extraocular muscle subnuclei that modu- late downward extraocular muscle tonus. Bilateral Arch Ophthalmol. 2001;119:1307-1314 RIMARY oblique muscle over- tropia but no other overt neurologic ab- action is a common ocular normalities. Surgical weakening of the motility disorder character- overacting oblique muscles improves ver- ized by vertical incomitance sions, eliminates the associated A or V pat- of the eyes in lateral gaze.1 In tern, and reduces torsion. Pprimary inferior oblique muscle overac- In 1916, Ohm6-8 postulated that pat- tion, an upshoot of the adducting eye oc- tern strabismus and oblique muscle over- curs when gaze is directed into the field of action may be due to abnormal vestibu- action of the inferior oblique muscle, pro- lar innervation. Almost a century later, a ducing a greater upward excursion of the unifying neurologic mechanism to ex- adducted eye than of the abducted eye.1 The plain primary oblique muscle overaction opposite occurs in primary superior ob- remains elusive. This ocular motor phe- lique muscle overaction. Although duc- nomenon seems to defy fundamental prin- tions appear to be normal and there is no ciples of physiology since nowhere else in evidence of yoke muscle paresis, alternate the body do individual muscles bilater- cover testing discloses a vertical tropia of ally overact. similar magnitude in the abducting eye. Pri- The primary function of the oblique From the Departments of mary inferior oblique muscle overaction is muscles in lower vertebrates such as fish Ophthalmology and Pediatrics, usually associated with ocular extorsion and is to counterrotate the eyes torsionally in University of Arkansas for V-pattern strabismus, whereas primary su- response to pitch (fore-and-aft) move- Medical Sciences, Little Rock perior oblique muscle overaction is usu- ments of the body.9,10 As a fish pitches its (Dr Brodsky); and the ally associated with ocular intorsion and A- body to swim upward or downward, a Departments of Ophthalmology 2-5 and Visual Sciences, Pediatrics, pattern strabismus. Superior oblique compensatory “wheel” rotation of the eyes and Neurology, Vanderbilt muscle overaction is often accompanied by is produced by the oblique muscles in re- 9 University School other neurologic disease, whereas inferior sponse to vestibular stimulation. The ex- of Medicine, Nashville, Tenn oblique muscle overaction generally oc- istence of this physiologic oblique muscle (Dr Donahue). curs in children who have congenital eso- overaction in lower animals led us to ques- (REPRINTED) ARCH OPHTHALMOL / VOL 119, SEP 2001 WWW.ARCHOPHTHALMOL.COM 1307 ©2001 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 organs).12,13 This hypothesis explains how sensory in- formation collected by the eyes can help to govern ex- traocular muscle tonus. The bilateral positioning of the eyes and ears permits them to function as balance or- gans. Visual and graviceptive input are yoked together A B within the central vestibular system to determine opti- mal postural orientation. In his early pioneering studies of vision-dependent tonus responses in fish, von Holst14 found that a poste- rior shift of a dorsal light source induces a pitch-up move- ment of the body, whereas an anterior shift induces a pitch-down movement, as if the animal is programmed to position the body so that the light source retains a dor- sal orientation (Figure 1). With the body stabilized in C D the upright position, an overhead light moving fore-and- aft evokes a wheel-turning movement of both eyes, which rotate to maintain torsional alignment with the light source (Figure 1).14-16 Since light normally comes from over- head when a fish is upright, a posterior movement of the light is registered as a pitch forward movement of the body (ie, a movement of the body away from the light). This change in visual input evokes increased tonus to the in- E F ferior oblique muscles, which extort the eyes (Figure 1). Figure 1. Physiologic effects of gravistatic (postural) and visual input to the The observation that visual and vestibular input can al- oblique muscle tonus in fish. These bilateral torsional eye movements function ter postural and extraocular muscle tonus to produce a to align the eyes with the perceived visual vertical by modulating oblique muscle physiologic bilateral oblique muscle overaction in lower tonus. A, A pitch-down body movement evokes increased inferior oblique muscle tonus and extorsion of the eyes. B, A pitch-up movement evokes animals suggests that similar excitatory stimuli may be increased superior oblique muscle tonus and intorsion of the eyes. C, In the operative in strabismic humans with primary oblique unrestrained fish, an anterior light source evokes a pitch-down body movement. muscle overaction. D, In the unrestrained fish, a posterior light source evokes a pitch-up body movement. E, In the restrained fish, anterior movement of overhead light evokes increased superior oblique muscle tonus and intorsion of both eyes. VESTIBULAR INTERACTIONS WITH F, In the restrained fish, posterior movement of overhead light evokes THE OCULAR MOTOR SYSTEM increased inferior oblique muscle tonus and extorsion of both eyes. To understand why primary oblique muscle overaction so tion whether a central vestibular imbalance in the pitch often accompanies early-onset strabismus, it is instruc- plane might offer an explanation for the occurrence of tive to examine the components of central vestibular tone primary oblique muscle overaction in humans. Clinical that influence eye position. The primary function of the observations suggest that an imbalance in central ves- vestibuloocular system is to maintain eye position and sta- tibular premotor output to the extraocular muscle sub- bilize fixation during head movements.16 Vestibulo- nuclei can produce the primary oblique muscle overac- ocular movements are the most primitive of all extraocu- tion that accompanies congenital strabismus. This central lar movements. As expounded by Walls, vestibular imbalance develops when early loss of bin- ocular vision or neurologic disease alters central vestibu- . the primitive function of the eye muscles was not to aim lar output in the pitch plane to produce excessive tonus the eyes at all. Their original actions were all reflex and invol- of the extraocular muscles that elevate the eyes (in the untary, and were designed to give the eyeball the attributes of a gyroscopically-stabilized ship, for the purpose of maintain- case of congenital esotropia and inferior oblique muscle ing a constancy of the visual field despite chance buffetings and overaction) or depress the eyes (in the case of neuro- twistings of the animals body by water currents.9(p303) logic disease and superior oblique muscle overaction). In the rabbit, for example, a rightward body tilt along CENTRAL TONUS MECHANISMS FOR its long axis causes the right eye to be lower in space than PRIMARY OBLIQUE MUSCLE OVERACTION the left eye. This tilt elicits a compensatory vertical diver- gence of the eyes to elevate the right eye and depress the The term tonus was originally coined by Ewald11 to de- left eye, thereby stabilizing the eyes in space.17-19 A pitch scribe the state of excitation of a living muscle during forward of the body would produce a compensatory ex- rest. In 1977, Meyer and Bullock12 advanced their tonus torsional movement of both eyes.14,15,20 hypothesis, which states that neuronal tonus pools within Now consider the same pitch-down body movement the central nervous system receive multisensory input and in a rabbit that is fixating with the right eye maximally ab- that tonus asymmetries between antagonistic pools can ducted and the left eye maximally adducted (Figure 2). produce tonic motor responses. According to this hy- Since the eyes are laterally placed in the rabbit, this posi- pothesis, the eyes are not merely sensory organs but tion of gaze would direct the left visual axis anterior to its components of a multimodally driven tonus pool that neutral position and the right visual axis posterior to its calibrates baseline muscle tone (ie, tonus-inducing neutral position. A forward pitch in the body plane with (REPRINTED) ARCH OPHTHALMOL / VOL 119, SEP 2001 WWW.ARCHOPHTHALMOL.COM 1308 ©2001 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 Midline Optic Axis Superior Oblique 51° Superior Rectus 23° Anterior 41° Semicircular Canals 56° Posterior Top View Figure 2. Overhead view of a rabbit fixating an object in the right posterior Figure 3. The close anatomical relationship of the semicircular canals and visual field. Solid lines correspond to the visual axis of the abducted right eye the extraocular muscles in humans is shown.