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Do You Really Need Your Oblique Muscles? Adaptations and Exaptations

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Do You Really Need Your Oblique Muscles? Adaptations and Exaptations SPECIAL ARTICLE Do You Really Need Your Oblique Muscles? Adaptations and Exaptations Michael C. Brodsky, MD Background: Primitive adaptations in lateral-eyed ani- facilitate stereoscopic perception in the pitch plane. It also mals have programmed the oblique muscles to counter- recruits the oblique muscles to generate cycloversional rotate the eyes during pitch and roll. In humans, these saccades that preset torsional eye position immediately torsional movements are rudimentary. preceding volitional head tilt, permitting instantaneous nonstereoscopic tilt perception in the roll plane. Purpose: To determine whether the human oblique muscles are vestigial. Conclusions: The evolution of frontal binocular vision has exapted the human oblique muscles for stereo- Methods: Review of primitive oblique muscle adapta- scopic detection of slant in the pitch plane and nonste- tions and exaptations in human binocular vision. reoscopic detection of tilt in the roll plane. These exap- tations do not erase more primitive adaptations, which Results: Primitive adaptations in human oblique muscle can resurface when congenital strabismus and neuro- function produce rudimentary torsional eye move- logic disease produce evolutionary reversion from exap- ments that can be measured as cycloversion and cyclo- tation to adaptation. vergence under experimental conditions. The human tor- sional regulatory system suppresses these primitive adaptations and exaptively modulates cyclovergence to Arch Ophthalmol. 2002;120:820-828 HE HUMAN extraocular static counterroll led Jampel9 to con- muscles have evolved to clude that the primary role of the oblique meet the needs of a dy- muscles in humans is to prevent torsion. namic, 3-dimensional vi- So the question is whether the human ob- sual world. Under normal lique muscles retain only a vestigial func- Tconditions, the extraocular muscles are tion in which they are consigned to make choreographed to an ensemble of visual a nominal contribution to vertical gaze, or tracking, refixation movements, and ver- whether the primary function of the hu- gence modulation that assures stable bin- man oblique muscles is to modulate tor- ocular fixation.1 But a fundamental di- sional eye position and to maintain per- chotomy defines the central programming ceptual stability of the visual world. of the human ocular motor plant. While the rectus muscles produce large ocular ro- PRIMARY ADAPTATIONS IN tations into secondary and tertiary posi- OBLIQUE MUSCLE FUNCTION tions of gaze, the oblique muscles evoke very limited torsional excursions of the To address this basic question, one must eyes.1 With rare exceptions,2 large tor- first examine the role of the oblique sional eye movements cannot be gener- muscles in lower animals. The extraocu- ated by normal individuals in the ab- lar muscles originally functioned to sta- sence of a head movement.3-7 This disparity bilize the eyes in space during body move- is also seen with vestibular eye move- ments and corresponding rotations of the ments in which a horizontal or vertical visual environment. In lateral-eyed verte- head rotation induces an ocular counter- brates such as fish and rabbits, the ob- From the Departments of rotation that effectively stabilizes the po- lique muscles produce torsional move- Ophthalmology and Pediatrics, sition of the eyes in space, but a head tilt ments of the eyes in response to pitch University of Arkansas for in the roll plane evokes a static ocular movements of the body.10,11 When the Medical Sciences, Little Rock. counterroll of only 10%.8 This negligible animal pitches forward or backward, the (REPRINTED) ARCH OPHTHALMOL / VOL 120, JUNE 2002 WWW.ARCHOPHTHALMOL.COM 820 ©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 oblique muscles produce a partial conjugate torsional rotation of the rent use, but as a consequence of (ex) wheel-like counterrotation of both globes producing extorsion or in- properties built for other reasons.30 eyes that helps to stabilize the tor- torsion of both eyes) and cyclover- According to this definition, a sional position of the eyes in sion1,7 (a conjugate torsional rota- mechanism must have a function space.10,11 In fish, a directional shift tion of both globes producing and must enhance the fitness of its in overhead luminance in the sagit- intorsion of one eye and extorsion bearer to qualify as an exapta- tal plane also produces an ipsidirec- of the other eye). These 2 torsional tion.30,31 For example, the feathers of tional pitch movement of the body eye movements in humans corre- birds may have originally evolved for (ie, a dorsal light reflex in the pitch spond to the torsional eye move- thermal insulation (an adaptation), plane).11-13 When the animal’s body ments in lower animals induced by only to be subsequently co-opted for is restrained during this stimulus, pitch and roll. Since pitch evokes a flight (an exaptation).31,32 this dorsal light reflex causes both disconjugate torsional rotation (ie, eyes to rotate torsionally so that their either intorsion or extorsion of both Cyclovergence, Stereoscopic upper poles move in the same di- eyes) in lateral-eyed animals, phy- Perception, and the Pitch Plane rection as the light source.12,13 Tor- logenetic retention of this primi- sional optokinetic nystagmus has tive adaptation in humans would According to Blakemore et al,32 bin- also been recorded in the rabbit, in- mean that a pitch stimulus (a slant ocular animals have abandoned the dicating that environmental rota- of the visual environment around the enormous biologic advantage of pan- tion in the pitch plane can directly interaural axis) would evoke a cy- oramic vision in order to have their activate the oblique muscles.14 clovergence response (a disconju- eyes pointing forward, the most ob- The oblique muscles also con- gate torsional movement of both vious advantage of which is stere- tribute to ocular movements dur- eyes) in humans, whereas a roll opsis. Frontal repositioning of the ing roll (ie, rotations about the head- stimulus (a tilt of the head or the vi- eyes seems to have exapted the ob- tail axis of the animal).15 A body tilt sual environment around the naso- lique muscles to subserve stereop- evokes utricular innervation to the occipital axis) would evoke a cyclo- sis. Evolution has grafted a new ipsilateral superior rectus and supe- version response in humans. These torsional control system that is sub- rior oblique muscles (which are el- primitive adaptations are indeed ordinate to binocular vision on top evators in fish and rabbits) and the measurable in the laboratory as the of the “primitive” dynamic tor- contralateral inferior rectus and in- small cyclovergence movements that sional programming of the oblique ferior oblique muscles (which are de- are induced artificially by haplos- muscles. Although the brain pro- pressors in fish and rabbits).16 The copy or optically induced cyclodis- grams eye torsional position by regu- resulting supraduction of the lower parity6,20-24 and in the small cyclo- lating the tonus of all extraocular eye and infraduction of the higher version movements that are evoked muscles, the oblique muscles have eye helps to stabilize the vertical po- by head tilt (ie, the human ocular the predominant effect on ocular tor- sition of the eyes during body roll. counterroll to a graviceptive stimu- sion. It is therefore instructive to ex- The magnitude of the ocular coun- lus),16 by torsional optokinetic amine torsional eye position as a terroll relative to a body roll is only stimuli,25-27 or by static-tilted visual function of oblique muscle inner- approximately 50% in lateral-eyed stimuli.28,29 vation. animals such as rabbits.17 A similar How do the human oblique vertical divergence can also be in- OBLIQUE MUSCLE muscles subserve stereopsis? Un- duced by a rotating optokinetic cyl- EXAPTATIONS der conditions of binocular fixa- inder rotating around the long axis tion, an object closer in space than of the fish10 or by providing un- From Visual Panorama to Frontal the fixation point will produce an equal visual input to the 2 eyes.11,14 Binocular Vision image on the temporal retinas, while For example, increasing visual in- an object farther in space than the put to the left eye of a fish by shin- Although we retain our primitive ad- fixation point will produce an im- ing a light at an angle onto the top aptations, the function of the hu- age on the nasal retinas.6 This hori- of a fish tank produces a body tilt to- man oblique muscles has evolved to zontal disparity forms the basis for ward the left in the freely swim- meet the needs of single binocular stereoscopic perception. If one ex- ming fish (a dorsal light reflex in the vision. In the course of evolution, amines the circles that appear el- roll plane). When body roll is re- primitive adaptations give way to ex- evated on a Titmus stereoacuity test strained, the same stimulus evokes aptations. An adaptation is some- under binocular conditions, exami- a vertical divergence of the eyes (su- thing fit (aptus) by construction for nation with each eye will show a na- praduction of the right eye and in- (ad) its usage.30 Exaptation is a rela- sal displacement of the circle in fraduction of the left) that tends to tively new evolutionary concept ad- space, indicating that the image falls equalize visual input to the 2 eyes.18 vanced by Gould30 to describe a fea- on the temporal retina in each eye These primitive adaptations use vi- ture, now useful to an organism, that when the circle is viewed binocu- sual and graviceptive input to set did not arise as an adaptation for its larly. When the Titmus test is turned postural and extraocular muscle to- present role, but that was subse- upside down so that the monocular nus during pitch and roll.19 quently co-opted for its current func- image falls on the nasal retinas of Human ocular torsion can be tion.
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