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 exaptations 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 torsional 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- conditions,T 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 movements 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

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©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. Such structures are fit (aptus) each eye, the circles appear to lie be- subdivided into cyclovergence (a dis- not by explicit molding for (ad) cur- hind the plane of the page.

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 A sensory (as opposed to a motor) basis, the single line will suddenly appear to be stereoscopically slanted in the pitch plane, with the upper pole inclined toward the observer and the lower pole inclined away from the observer. The opposite inclination is seen when the upper poles of the Maddox Rods are rotated temporally. The original trea- tise by Wheatstone34 describing his invention of the stereoscope in 1838 provided the first example of pitch stereopsis produced by dichoptic lines that are tilted in different di- rections. This stereoscopic effect shows us something remarkable about the B normal binocular visual system. It tells us that when an isolated vertical image cyclodisparity falls within the physiologic range of sensory fusion, it is misregistered stereoscopically as a slant of the vertical object in the pitch plane.7,21,22,32-38 In a real world setting, however, perceived pitch is not solely a function of retinal cyclodisparity, but it depends both on the brain’s computation of Left Eye Right Eye registered eye rotation and on retinal cyclodisparity. So to create an ac- Figure 1. Tilt is the monocular correlate of stereoscopic slant. A, An individual binocularly viewing a curate stereoscopic representation of vertical object that is slanted in the pitch plane. B, The monocular images corresponding to the object are extorted when viewed with each eye. vertical objects in the pitch plane, cyclovergence should not occur and the eyes must be locked into a well- Now consider a binocular in- be seen if there were intorsion of defined static orientation relative to dividual with normal stereopsis who each eye. a given gaze position (ie, conform- is fixating on the center of a verti- If a vertical cyclodisparity in the ing to Donder’s law).1,7,21,22 The in- cal object that is slanted so that its 2 eyes is translated by the visual cor- nervational patterns of oblique inferior aspect is closer than the su- tex into a binocular sensation of muscle recruitment, which coun- perior aspect (Figure 1). As the in- depth in the pitch plane (ie, slant), teract the torsional actions of the rec- dividual fixates the center of the can retinal image torsion cause a ver- tus muscles in different positions of slanted object, the visual image of the tical binocular image to be per- gaze, must also be subordinate to this upper pole is postfixational, which ceived as slanted in the pitch plane? goal. means that it falls onto the nasal The answer is yes. The reader can ap- That binocular torsional con- retina of each eye, whereas the vi- preciate this phenomenon by plac- trol represents an active function of sual image of the lower pole is pre- ing a white Maddox Rods over each the human oblique muscles rather fixational, falling onto the tempo- of the 2 eyes in a trial frame, and than an evolutionary loss of con- ral retina of each eye. The reader can looking toward a bright focal light tractile function is seen in the kine- appreciate this slant illusion by hold- source with the grids oriented hori- matics of human convergence.39 It ing a pencil in the midsagittal plane zontally to produce a vertical line has long been recognized that both with the upper pole slanted away (Figure 2). Now counterrotate the eyes extort during convergence and from the body and the lower pole lenses so that their upper pole of that this extorsion increases in tilted toward the body. On occlu- each line moves nasally and their downgaze and decreases in up- sion of either eye, the upper pole of lower pole moves temporally until gaze.40,41 (Extorsion is even consid- the pencil will appear to be tilted, the image of the binocular vertical ered by some to be a component of with the upper pole leaning toward line breaks into 2 tilted lines (Fig- the synkinetic near reflex.42) While the side of the uncovered eye (Fig- ure 2). If the rotation is stopped at the existence of these cyclover- ure 1).33 So under monocular con- the break point, the torsional dip- gence movements were once ditions, the person perceives a dis- lopia can be overcome and the 2 lines thought to constitute a violation of conjugate image torsion that is can be fused. When cyclofusion oc- Listing’s law, they can be recon- analogous to how the image would curs, which is almost purely on a ciled with Listing’s law if it is as-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 sumed that convergence is associ- A ated with a temporal rotation of Listing’s plane in each eye (Figure 3).43 Vertical rotation of the eyes around these temporally rotated axes produces incyclover- gence of the eyes in upgaze and ex- cyclovergence in downgaze.44-46 Several lines of evidence suggest a neural and biomechanical basis for these cyclovergence movements. In monkeys, Mays et al47 measured single cell recordings within the trochlear nucleus and found de- Right Eye Left Eye creased unit activity during convergence. This decrease in firing rate was greater when the monkey con- verged in downgaze than in up- B gaze, a finding that corresponds to the observed convergence-associated torsional movements in humans. More recently, dynamic mag- netic resonance imaging by Demer et al48,49 have found that downward rotation of the lateral rectus muscle pulley and medial rotation of the inferior rectus pulley during convergence, indicating that the inferior oblique muscle may also play a role in convergence-associated torsion, presumably via its collagenous attach- ments to the lateral rectus and inferior rectus muscles. From an evolutionary perspec- Figure 2. Binocular cyclodisparity of vertical lines is perceived stereoscopically as slant. A, Rotation of tive, it is worth examining whether horizontal double Maddox Rods to produce binocular image intorsion (as would be seen if both eyes these torsional movements during were extorted). B, Sensory cyclofusion causes the patient to stereoscopically perceive a vertical line (solid convergence simply represent primi- line) as slanted in the pitch (ie, sagittal) plane (dashed line). tive adaptations that have been phy- logenetically retained, like the small ocular horizontal disparities that holtz.40) In convergence, the in- ocular counterroll which has no produce stereoscopic perception in creased intorsion of the eyes in up- known function in humans.17 In the different positions of vertical gaze.51 gaze and extorsion in downgaze lateral-eyed animal, upgaze corre- This exaptation serves to minimize helps to torsionally align the hori- sponds to an intorsional move- the brain’s computational load for zontal meridians of the eyes with ment of both eyes when the rota- stereoscopic perception.51 their respective horizontal visual tion is viewed from the frontal Human cyclovergence is most landmarks, thereby facilitating ste- perspective, while downgaze corre- robust at near fixation, where it plays reopsis. Since convergence is gen- sponds to an extorsional rotation of an active role in stereoscopic vi- erally used for downgaze, where near both eyes. One could argue that con- sion. If convergence were not linked objects are situated, the innerva- vergence in humans may simply to cyclovergence, symmetrical con- tional link between convergence and stress the system to a degree that pre- vergence on a frontoparallel plane extorsion presumably serves to set vents binocular suppression of these would induce incyclodisparity of the the operational position for stere- primitive rotations. However, re- horizontal images in upgaze and ex- opsis as slightly in downgaze, where cent studies suggest that the fron- cyclodisparity of the horizontal im- near objects can be held by the arms tal binocular visual system has ages in downgaze for each eye, solely and illuminated by overhead latched on to this primitive tor- on the basis of the geometric angle light.40,41,52 Although the torsional sional bias and exapted it to sub- from which each eye views a planar movements associated with conver- serve stereoscopic perception in the surface. (The opposite cyclodispar- gence are preprogrammed,17 they ex- pitch plane.50,51 To subserve stere- ity bias occurs for vertical visual hibit remarkable plasticity53 and are opsis, the oblique muscles have been landmarks due to projection geom- enhanced by the depth perception exapted to torsionally align the eyes etry; however, it is reduced or re- of stereograms,54 demonstrating that with their corresponding visual im- versed by the horizontal retinal shear they also rely on visual input to more ages in a way that preserves the bin- that was described by Helm- accurately subserve the needs of bin-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 A landmarks would induce a misper- ception of stereoscopic slant for vertical lines. For any position of gaze, the oblique muscles must torsionally anchor the eyes to produce a stable motor substrate for slant perception of vertical objects. Psychophysical experiments have shown that horizontal visual D D landmarks are selectively used in humans to lock in torsional eye posi- LP LP tion, although the neural feedback U U loops for this process are un- known. As early as 1861, Nagel35 observed that the rotation of horizontal fusion contours produced B cyclovergence, while the rotation of vertical contours produced only a stereoscopic effect.28 Ogle and Eller- brock37 noted that cyclofusion of torsionally disparate horizontal lines that were presented dichoptically with no visual background caused a previously fused vertical line to pitch in the sagittal plane. Accord- ing to Bradshaw and Rogers,57 cy- D D clovergence is not well driven by disparities along vertical meridians even when these are created by a real in- U U clined surface. By inducing cyclodisparity of horizontal lines to the 2 eyes dichoptically, small cyclofu- D D sional eye movements can be elicited in humans under experimen- LP LP tal conditions.7,20,23,24,37,38,56 The small U U size of these cyclofusional movements suggests that the human cyclovergence system is equipped to Figure 3. View of both eyes from above demonstrating orientation of Listing’s plane (LP) during distance provide a fine-motor modulation to fixation (A) and convergence (B). Curved arrows denote cyclovergence movements of the eyes associated with vertical rotation about horizontal visual axes in Listing’s plane. A “saloon door” rotation of Listing’s a system that is designed primarily plane, which is opposite in direction to the ocular rotation, can be used to reconcile the for stability rather than move- convergence-associated extorsion of the eyes in downgaze (D) and intorsion of the eyes in upgaze (U) ment.7 The greater stereoscopic value with Listing’s law. of vertically compared than horizontally tilted images explains why ocular vision and depth percep- entation selectivity during simulta- vertically oriented gratings evoke tion. Without these torsional move- neous binocular stimulation. Cer- smaller cyclovergence movements ments, convergence during vertical tain binocular cells responded than horizontally oriented grat- gaze would limit optimal stereo- specifically to objects tilted in 3-di- ings.23 scopic perception to 1 gaze eleva- mensional space toward the cat or Humans inhabit a terrestrial en- tion, requiring repositioning of the away from it.32 Such binocular cells vironment composed of primarily head to optimize depth perception may form at least part of the sub- vertical and horizontal landmarks of targets at different earth eleva- strate for sensory cyclofusion in hu- that serve as reference points for ver- tions. Thus, this oblique muscle ex- mans. The survival value of stereo- tical orientation.21,22 In a terrestrial aptation provides the luxury- scopic spatial orientation explains setting, the most prominent hori- optimizing stereopsis for targets at why cyclofusional movements are so zontal contour is the horizon, which different eye elevations without the limited in primary gaze and why sen- may be the main visual reference for necessity of head movements in the sory cyclofusion is so well devel- stabilizing the eyes relative to the pitch plane. oped.3-7,55,56 Sensory cyclofusion outside world.21 While cyclodispari- Almost 30 years ago, Blake- without motor cyclofusion is a pre- ties of vertical contours may be more et al32 recorded action poten- requisite for pitch stereopsis (ie, slant caused by slant of the observed ob- tials from binocular neurons in the perception). Motor cyclofusion of jects, cyclodisparities of horizontal cat’s visual cortex and measured ori- these torsionally disparate vertical contours indicate cyclovergence er-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 20,21 rors that need correction. As sum- A marized by Howard and Rogers33: An orientation disparity between the images of lines in the horizontal plane of regard can be due only to eye misalignment, whereas an orientation disparity from a vertical line may be due to inclination of the line in depth. It would therefore be adaptive if cyclovergence were evoked only by disparities in horizontal elements, leaving residual disparities in vertical elements intact as clues for inclination. Right Eye Left Eye If cyclodisparities in horizontal visual landmarks of the visual scene that occur at low stimulus frequencies and low amplitudes serve as the physiologic stimulus for cyclovergence as B proposed by Howard and Zacher,58 then horizontal cyclofusion must serve to torsionally anchor the eyes, allowing the visual cortex to extract and construct a stable and reproduc- ible representation for pitch stereopsis.7 By using cyclodisparity of horizontally oriented lines as the feedback signal for torsional misalignment of the eyes and allowing cyclodisparity of vertically oriented lines to signal depth (ie, slant), the brain can re- cruit the oblique muscles to control cyclovergence and thereby assure ac- curate stereoscopic perception of vertical objects in the pitch plane. While a cyclodisparity of horizontal lines are Figure 4. Right superior oblique palsy. A, Examiner’s view of patient’s retinas showing extorsion of the the driving force for this cyclofu- right eye. B, Under binocular conditions, the patient perceives a vertical object (solid line) as sional reflex, stereopsis and vertical stereoscopically slanted in the pitch plane (dashed line). visual orientation are its emergent functions. As seen in superior oblique be remembered that sensory fusion of If a binocular vertical cyclodis- palsy, the concept of Panum’s space torsional images can cause vertical ob- parity produces a stereoscopic sen- can be extrapolated to torsional eye jects to be perceived as slanted. Psy- sation of pitch, then ocular torsion position. Ocular torsion within the chophysical experiments by Howard produced by cyclovertical muscle realm of fusion induces an illusory and Kaneko62 have shown that an iso- palsy should produce an abnormal pitch stereopsis of isolated vertical lated shear disparity of vertical lines sensation of pitch stereopsis. Not lines, while torsion outside the realm will induce a stereoscopic slant, surprisingly, abnormal pitch stere- of fusion induces torsional diplopia whereas a cyclodisparity that twists opsis is a common symptom of ac- in the roll plane.5,60,61 Ocular torsion both vertical and horizontal lines will quired superior oblique palsy. Lind- of 5°, as generally occurs with uni- not induce a perceived slant of the vi- blom et al59 found that adults with lateral superior oblique palsy, is not sual environment. These experi- acquired unilateral or bilateral su- an impediment to fusion, whereas ments would predict that patients perior oblique palsy perceived the ocular torsion of more than 10°, with unilateral superior oblique palsy upper pole of a vertical rod as being which accompanies bilateral supe- and extorsion of 1 eye would stereo- tilted toward them in the sagittal rior oblique palsy, precludes fu- scopically perceive isolated visual plane under binocular conditions. sion.6 In unilateral superior oblique landmarks in the sagittal plane as This stereoscopic illusion corre- palsy, it is often stated that strabis- slanted toward them. sponded to the associated extor- mus surgery or prismatic correction sion of the paretic eye (Figure 4). to vertically realign the eyes is suffi- Cycloversion, Nonstereoscopic Subjects also perceived the un- cient to restore cyclofusion, even Perception, and the Roll Plane fused image corresponding to the eye when the extorsion persists in the pal- with the superior oblique palsy as in- sied eye. However, the persistence of Unlike cyclovergence, which is re- torted (ie, tilted in the roll plane) extorsion in one eye is not without markably stable and seems to de- relative to the other image. perceptual consequence, and it should pend primarily on where the eyes are

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Figure 5. Depiction of torsional eye position during head tilt from side to side. (1) Initial torsional position during right head tilt. (2) During head tilt to the left, the eyes lead the head and quickly assume their final torsional position corresponding to the left head tilt. (3) The eyes “hang in space” until the head catches up. (4) Head tilt to the right produces the reverse sequence of torsional eye movements. (Reprinted with permission from The American Association for the Advancement of Science, copyright 1999.63)

looking, human cycloversion shows plane. The 3-dimensional scleral the ancestral control system that pro- both intrasubject and intersubject search coil recordings were per- duces the ocular counterroll variation.39 These findings impli- formed as normal study partici- (Table). Similar torsional saccades cate different neural control strate- pants observed a laser spot while have not been observed in lateral- gies for cycloversion and cyclover- their eyes were directed 20° down- eyed animals (although studies in- gence.39 One explanation for this ward. The subjects then made com- volving eye-head or eye-body coor- disparity is that cycloversion is prob- bined eye-head movements to refix- dination in animals are extremely ably not as important to stereo- ate the laser spot as it jumped 20° difficult to perform). scopic vision as cyclovergence, (from right head tilt and right gaze which determines stereoscopic vol- to left head tilt and left gaze). Eye Reversion From Exaptation ume at any given pitch plane, alters movement recordings showed that to Adaptation slant perception of vertical objects, these subjects generated ipsiver- and is necessary for stereo con- sive torsional saccades that ranged Since ocular torsion within the realm stancy.39 in size from 11° to 17° and aver- of fusion can produce a stereo- Nevertheless, large cyclover- aged 14.5°. These cycloversional eye scopic tilt in the pitch plane, it seems sional movements of the eyes cre- movements preceded the head reasonable to ask whether strabis- ate a problem for stereoscopic per- movements by 20 to 60 millisec- mus or other neurologic disease, ception. Misslisch et al17 have argued onds, indicating that these move- which can be associated with a that the superimposition of a primi- ments were not vestibular in ori- pathologic tilt in the internal repre- tive cycloversion movement of the gin. The eyes arrived at the target sentation of the gravitational verti- eyes (such as an ocular counterroll first and locked on, hanging in space cal, could recalibrate prenuclear in- evoked by a head tilt) on conver- as the head rotated around them nervation to the extraocular muscles gence would induce a cyclodispar- (Figure 5). When the head came and produce a torsional deviation of ity and disrupt stereoacuity. The to a halt, the ocular torsion relative the eyes that conforms to this inter- brain strikes a balance between gy- to the head had stabilized near zero, nal shift. Again, the answer is yes. roscopic and stereoptic mecha- and the eyes were poised for the One of the primitive functions of the nisms by damping the ocular coun- swiftest possible response to fur- human oblique muscles is to rotate terroll by approximately 70% in ther movement of the target. These the eyes toward the subjective vi- convergence.18 In this way, exapta- torsional eye movements, which oc- sual vertical; when this internal rep- tions of the neural circuitry that cur at the initiation of a head tilt and resentation is altered under patho- steers our cyclovergence and cyclo- are not visible on gross inspection, logic conditions, ocular torsion is the version movements seem to over- may reveal another exaptation of our inevitable result. In humans, as in ride our primitive adaptations to pro- torsional control system. The hu- lower animals, the central vestibu- mote stereopsis.39,50 man oblique muscles may have been lar system uses weighted input from While the human oblique exapted to generate saccadic tor- the 2 labyrinths and weighted vi- muscles function under static con- sional eye movements to reestab- sual input from the 2 eyes to estab- ditions to constrain torsional rota- lish roll plane orientation in antici- lish subjective vertical orientation in tion of the eyes, it is not the physi- pation of a postural rotation in the pitch and roll.64,65 In humans, cyclo- ologic role of any muscle to simply roll plane. These anticipatory sac- version is evoked by visual or gravi- constrain movement (check liga- cades instantaneously recalibrate tor- ceptive imbalance in the roll plane,64 ments and muscle pulleys are bet- sional eye position to provide a stable whereas cyclovergence is evoked by a ter suited to this function). To the visual representation of tilt in the roll visual or graviceptive imbalance in the surprise of many, Tweed et al63 have (frontal) plane. The evolution of pitch plane.65 In the roll plane, uni- recently found that the human ob- frontally positioned eyes for stere- lateral loss of otolithic tone second- lique muscles execute large cyclo- opsis may have created a survival ad- ary to brainstem, cerebellar, or versional saccades immediately pre- vantage for the grafting of this new utricular injury causes skew devia- ceding head movements in the roll torsional control system on top of tion, whereas asymmetrical visual in-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 put in humans with congenital strabismus evokes dissociated vertical Oblique Muscle Adaptations and Exaptations divergence (Table).65 In skew deviation, unequal graviceptive tone from Adaptations Adaptations Exaptations (Lateral-Eyed Animals) (Humans) (Humans) the otoliths produces a pathologic tilt in the internal representation of the Cyclovergence visual vertical in the roll plane, which Pitch plane is associated with a corresponding torsional repositioning of both eyes Dorsal light reflex Primary oblique muscle Fusional cyclovergence (for and a vertical divergence of the eyes overaction pitch stereopsis) (Table).66 In dissociated vertical divergence, a dorsal light reflex in the Ocular counterroll Alternating skew deviation (torsional) roll plane is also associated with visually induced tilt in the subjective Cycloversion visual vertical, and the cyclover- Roll plane sional component is ipsidirectional to 67 the patient’s perceived visual tilt. Dorsal light reflex Dissociated vertical divergence Dissociated vertical divergence Since the cycloversional component (vertical component) (torsional component) of dissociated vertical divergence does not accompany the dorsal light re- Cycloversion to torsional optokinetic targets, static visual flex in lateral-eyed animals, and it can- tilt, binocular vertical disparity not be accounted for by anatomical repositioning of the extraocular Ocular counterroll Ocular counterroll (torsional), ? Anticipatory torsional muscles, this component of the hu- (vertical) skew deviation saccades man dorsal light reflex seems to represent an exaptation to restore vertical orientation during monocular vironment, and an altered torsional man oblique muscles generate a cy- viewing.67 Theassociatedcycloversion position of the eyes constitutes an cloversion movement of the eyes just movement that occurs when humans ocular motor recalibration to the tilted prior to volitional head movement to fuseverticallydisparateimages68,69 may or slanted internal representation of lock in a stable visual perception of indicate that binocular vertical dispar- the visual world that characterizes tilt. These exaptations provide spa- ity in humans is similarly misregis- central vestibular disease. By recog- tial accuracy and temporal continu- tered by the brain as tilt.70 nizing that a subjective tilt of the vi- ity to our stereoscopic visual percep- In the pitch plane, these same sual environment evokes a correction of slant and our nonstereoscopic primitive adaptations are operative. tive torsional repositioning of both visual perception of tilt. In a larger Donahue and I65 have proposed that eyes, we can begin to place the horse sense, they furnish us with a multi- primary oblique muscle overaction is before the cart in understanding con- faceted torsional control system that associated with a slant of the inter- genital strabismus. provides 3-dimensional stability to the nal representation of the visual ver- visual world and thereby improves tical in the pitch plane. A subjective CONCLUSIONS fitness. inclination of the superior portion of Exaptations in human oblique the visual environment toward the in- To understand why you really need muscle function do not completely dividual would produce a correspond- your oblique muscles, it is necessary erase more primitive adaptations. ing extorsion of both globes and lead to distinguish primitive adaptations, These primitive adaptations pro- to inferior oblique muscle overac- which originally evolved to stabilize duce the small vestigial torsional eye tion.65 Conversely, structural neuro- laterally placed eyes during body pitch movements that can be measured ex- logic disease within the brain stem or and roll, from exaptations, which sub- perimentally by inducing pitch or tilt cerebellum would produce the intor- sequently evolved to meet the needs of the external visual environment. sion and superior oblique muscle of frontal binocular vision. The hu- They manifest clinically when con- overaction so commonly seen in chil- man oblique muscles have been ex- genital strabismus or other central dren with Chiari malformations, me- apted to override primitive torsional vestibular disease alters our inter- ningomyelocele, or hydrocepha- adaptations with newer mecha- nal representation of the visual ver- lus.65 The alternating skew deviation nisms that subserve stereopsis. These tical. One may conclude that only on lateral gaze with bilateral abduct- exaptations govern the relative tor- our primitive adaptations are vesti- ing hypertropia that is associated with sional alignment of the eyes in differ- gial; our oblique muscles are not. craniocervical disease may repre- ent positions of gaze. Since percep- sent another central vestibular dis- tion of stereoscopic slant is a function Submitted for publication June 7, 2001; turbance in the pitch plane.71,72 of torsional eye position, the human final revision received February 12, Under pathological conditions, oblique muscles modulate cyclover- 2002; accepted February 28, 2002. the oblique muscles still function to gence to establish a stable stereo- This study was supported in part keep the eyes in binocular torsional scopic pitch representation of the by a grant from Research to Prevent register with the perceived visual en- visual world. In the roll plane, the hu- Blindness, Inc, New York, NY.

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