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Figure 1.
Tilt is the monocular correlate of stereoscopic slant. A, An individual binocularly viewing a vertical object that is slanted in the pitch plane. B, The monocular images corresponding to the object are extorted when viewed with each eye.

Tilt is the monocular correlate of stereoscopic slant. A, An individual binocularly viewing a vertical object that is slanted in the pitch plane. B, The monocular images corresponding to the object are extorted when viewed with each eye.

Figure 2.
Binocular cyclodisparity of vertical lines is perceived stereoscopically as slant. A, Rotation of horizontal double Maddox Rods to produce binocular image intorsion (as would be seen if both eyes were extorted). B, Sensory cyclofusion causes the patient to stereoscopically perceive a vertical line (solid line) as slanted in the pitch (ie, sagittal) plane (dashed line).

Binocular cyclodisparity of vertical lines is perceived stereoscopically as slant. A, Rotation of horizontal double Maddox Rods to produce binocular image intorsion (as would be seen if both eyes were extorted). B, Sensory cyclofusion causes the patient to stereoscopically perceive a vertical line (solid line) as slanted in the pitch (ie, sagittal) plane (dashed line).

Figure 3.
View of both eyes from above demonstrating orientation of Listing's plane (LP) during distance 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 plane, which is opposite in direction to the ocular rotation, can be used to reconcile the convergence-associated extorsion of the eyes in downgaze (D) and intorsion of the eyes in upgaze (U) with Listing's law.

View of both eyes from above demonstrating orientation of Listing's plane (LP) during distance 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 plane, which is opposite in direction to the ocular rotation, can be used to reconcile the convergence-associated extorsion of the eyes in downgaze (D) and intorsion of the eyes in upgaze (U) with Listing's law.

Figure 4.
Right superior oblique palsy. A, Examiner's view of patient's retinas showing extorsion of the right eye. B, Under binocular conditions, the patient perceives a vertical object (solid line) as stereoscopically slanted in the pitch plane (dashed line).

Right superior oblique palsy. A, Examiner's view of patient's retinas showing extorsion of the right eye. B, Under binocular conditions, the patient perceives a vertical object (solid line) as stereoscopically slanted in the pitch plane (dashed line).

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.)

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)

Oblique Muscle Adaptations and Exaptations
Oblique Muscle Adaptations and Exaptations
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Special Article
June 2002

Do You Really Need Your Oblique Muscles?Adaptations and Exaptations

Author Affiliations

From the Departments of Ophthalmology and Pediatrics, University of Arkansas for Medical Sciences, Little Rock.

Arch Ophthalmol. 2002;120(6):820-828. doi:10.1001/archopht.120.6.820
Abstract

Background  Primitive adaptations in lateral-eyed animals have programmed the oblique muscles to counterrotate the eyes during pitch and roll. In humans, these torsional movements are rudimentary.

Purpose  To determine whether the human oblique muscles are vestigial.

Methods  Review of primitive oblique muscle adaptations and exaptations in human binocular vision.

Results  Primitive adaptations in human oblique muscle function produce rudimentary torsional eye movements that can be measured as cycloversion and cyclovergence under experimental conditions. The human torsional regulatory system suppresses these primitive adaptations and exaptively modulates cyclovergence to facilitate stereoscopic perception in the pitch plane. It also recruits the oblique muscles to generate cycloversional saccades that preset torsional eye position immediately preceding volitional head tilt, permitting instantaneous nonstereoscopic tilt perception in the roll plane.

Conclusions  The evolution of frontal binocular vision has exapted the human oblique muscles for stereoscopic detection of slant in the pitch plane and nonstereoscopic detection of tilt in the roll plane. These exaptations do not erase more primitive adaptations, which can resurface when congenital strabismus and neurologic disease produce evolutionary reversion from exaptation to adaptation.

THE HUMAN extraocular muscles have evolved to meet the needs of a dynamic, 3-dimensional visual world. Under normal conditions, the extraocular muscles are choreographed to an ensemble of visual tracking, refixation movements, and vergence modulation that assures stable binocular fixation.1 But a fundamental dichotomy defines the central programming of the human ocular motor plant. While the rectus muscles produce large ocular rotations into secondary and tertiary positions of gaze, the oblique muscles evoke very limited torsional excursions of the eyes.1 With rare exceptions,2 large torsional eye movements cannot be generated by normal individuals in the absence of a head movement.37 This disparity is also seen with vestibular eye movements in which a horizontal or vertical head rotation induces an ocular counterrotation that effectively stabilizes the position of the eyes in space, but a head tilt in the roll plane evokes a static ocular counterroll of only 10%.8 This negligible static counterroll led Jampel9 to conclude that the primary role of the oblique muscles in humans is to prevent torsion. So the question is whether the human oblique muscles retain only a vestigial function in which they are consigned to make a nominal contribution to vertical gaze, or whether the primary function of the human oblique muscles is to modulate torsional eye position and to maintain perceptual stability of the visual world.

PRIMARY ADAPTATIONS IN OBLIQUE MUSCLE FUNCTION

To address this basic question, one must first examine the role of the oblique muscles in lower animals. The extraocular muscles originally functioned to stabilize the eyes in space during body movements and corresponding rotations of the visual environment. In lateral-eyed vertebrates such as fish and rabbits, the oblique muscles produce torsional movements of the eyes in response to pitch movements of the body.10,11 When the animal pitches forward or backward, the oblique muscles produce a partial wheel-like counterrotation of both eyes that helps to stabilize the torsional position of the eyes in space.10,11 In fish, a directional shift in overhead luminance in the sagittal plane also produces an ipsidirectional pitch movement of the body (ie, a dorsal light reflex in the pitch plane).1113 When the animal's body is restrained during this stimulus, this dorsal light reflex causes both eyes to rotate torsionally so that their upper poles move in the same direction as the light source.12,13 Torsional optokinetic nystagmus has also been recorded in the rabbit, indicating that environmental rotation in the pitch plane can directly activate the oblique muscles.14

The oblique muscles also contribute to ocular movements during roll(ie, rotations about the head-tail axis of the animal).15 A body tilt evokes utricular innervation to the ipsilateral superior rectus and superior oblique muscles (which are elevators in fish and rabbits) and the contralateral inferior rectus and inferior oblique muscles (which are depressors in fish and rabbits).16 The resulting supraduction of the lower eye and infraduction of the higher eye helps to stabilize the vertical position of the eyes during body roll. The magnitude of the ocular counterroll relative to a body roll is only approximately 50% in lateral-eyed animals such as rabbits.17 A similar vertical divergence can also be induced by a rotating optokinetic cylinder rotating around the long axis of the fish10 or by providing unequal visual input to the 2 eyes.11,14 For example, increasing visual input to the left eye of a fish by shining a light at an angle onto the top of a fish tank produces a body tilt toward the left in the freely swimming fish (a dorsal light reflex in the roll plane). When body roll is restrained, the same stimulus evokes a vertical divergence of the eyes (supraduction of the right eye and infraduction of the left) that tends to equalize visual input to the 2 eyes.18 These primitive adaptations use visual and graviceptive input to set postural and extraocular muscle tonus during pitch and roll.19

Human ocular torsion can be subdivided into cyclovergence (a disconjugate torsional rotation of the globes producing extorsion or intorsion of both eyes) and cycloversion1,7 (a conjugate torsional rotation of both globes producing intorsion of one eye and extorsion of the other eye). These 2 torsional eye movements in humans correspond to the torsional eye movements in lower animals induced by pitch and roll. Since pitch evokes a disconjugate torsional rotation (ie, either intorsion or extorsion of both eyes) in lateral-eyed animals, phylogenetic retention of this primitive adaptation in humans would mean that a pitch stimulus (a slant of the visual environment around the interaural axis) would evoke a cyclovergence response (a disconjugate torsional movement of both eyes) in humans, whereas a roll stimulus (a tilt of the head or the visual environment around the naso-occipital axis) would evoke a cycloversion response in humans. These primitive adaptations are indeed measurable in the laboratory as the small cyclovergence movements that are induced artificially by haploscopy or optically induced cyclodisparity6,2024 and in the small cycloversion movements that are evoked by head tilt (ie, the human ocular counterroll to a graviceptive stimulus),16 by torsional optokinetic stimuli,2527 or by static-tilted visual stimuli.28,29

OBLIQUE MUSCLE EXAPTATIONS
From Visual Panorama to Frontal Binocular Vision

Although we retain our primitive adaptations, the function of the human oblique muscles has evolved to meet the needs of single binocular vision. In the course of evolution, primitive adaptations give way to exaptations. An adaptation is something fit (aptus) by construction for (ad) its usage.30Exaptation is a relatively new evolutionary concept advanced by Gould30 to describe a feature, now useful to an organism, that did not arise as an adaptation for its present role, but that was subsequently co-opted for its current function. Such structures are fit (aptus) not by explicit molding for (ad) current use, but as a consequence of (ex) properties built for other reasons.30 According to this definition, a mechanism must have a function and must enhance the fitness of its bearer to qualify as an exaptation.30,31 For example, the feathers of birds may have originally evolved for thermal insulation (an adaptation), only to be subsequently co-opted for flight (an exaptation).31,32

Cyclovergence, Stereoscopic Perception, and the Pitch Plane

According to Blakemore et al,32 binocular animals have abandoned the enormous biologic advantage of panoramic vision in order to have their eyes pointing forward, the most obvious advantage of which is stereopsis. Frontal repositioning of the eyes seems to have exapted the oblique muscles to subserve stereopsis. Evolution has grafted a new torsional control system that is subordinate to binocular vision on top of the "primitive" dynamic torsional programming of the oblique muscles. Although the brain programs eye torsional position by regulating the tonus of all extraocular muscles, the oblique muscles have the predominant effect on ocular torsion. It is therefore instructive to examine torsional eye position as a function of oblique muscle innervation.

How do the human oblique muscles subserve stereopsis? Under conditions of binocular fixation, an object closer in space than the fixation point will produce an image on the temporal retinas, while an object farther in space than the fixation point will produce an image on the nasal retinas.6 This horizontal disparity forms the basis for stereoscopic perception. If one examines the circles that appear elevated on a Titmus stereoacuity test under binocular conditions, examination with each eye will show a nasal displacement of the circle in space, indicating that the image falls on the temporal retina in each eye when the circle is viewed binocularly. When the Titmus test is turned upside down so that the monocular image falls on the nasal retinas of each eye, the circles appear to lie behind the plane of the page.

Now consider a binocular individual with normal stereopsis who is fixating on the center of a vertical object that is slanted so that its inferior aspect is closer than the superior aspect (Figure 1). As the individual fixates the center of the slanted object, the visual image of the upper pole is postfixational, which means that it falls onto the nasal retina of each eye, whereas the visual image of the lower pole is prefixational, falling onto the temporal retina of each eye. The reader can appreciate this slant illusion by holding a pencil in the midsagittal plane with the upper pole slanted away from the body and the lower pole tilted toward the body. On occlusion of either eye, the upper pole of the pencil will appear to be tilted, with the upper pole leaning toward the side of the uncovered eye (Figure 1).33 So under monocular conditions, the person perceives a disconjugate image torsion that is analogous to how the image would be seen if there were intorsion of each eye.

If a vertical cyclodisparity in the 2 eyes is translated by the visual cortex into a binocular sensation of depth in the pitch plane (ie, slant), can retinal image torsion cause a vertical binocular image to be perceived as slanted in the pitch plane? The answer is yes. The reader can appreciate this phenomenon by placing a white Maddox Rods over each of the 2 eyes in a trial frame, and looking toward a bright focal light source with the grids oriented horizontally to produce a vertical line (Figure 2). Now counterrotate the lenses so that their upper pole of each line moves nasally and their lower pole moves temporally until the image of the binocular vertical line breaks into 2 tilted lines (Figure 2). If the rotation is stopped at the break point, the torsional diplopia can be overcome and the 2 lines can be fused. When cyclofusion occurs, which is almost purely on 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 treatise 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 directions.

This stereoscopic effect shows us something remarkable about the 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.7,21,22,3238 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 registered eye rotation and on retinal cyclodisparity. So to create an accurate stereoscopic representation of vertical objects in the pitch plane, cyclovergence should not occur and the eyes must be locked into a well-defined static orientation relative to a given gaze position (ie, conforming to Donder's law).1,7,21,22 The innervational patterns of oblique muscle recruitment, which counteract the torsional actions of the rectus muscles in different positions of gaze, must also be subordinate to this goal.

That binocular torsional control represents an active function of the human oblique muscles rather than an evolutionary loss of contractile function is seen in the kinematics of human convergence.39 It has long been recognized that both eyes extort during convergence and that this extorsion increases in downgaze and decreases in upgaze.40,41(Extorsion is even considered by some to be a component of the synkinetic near reflex.42) While the existence of these cyclovergence movements were once thought to constitute a violation of Listing's law, they can be reconciled with Listing's law if it is assumed that convergence is associated 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 incyclovergence of the eyes in upgaze and excyclovergence in downgaze.4446 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 decreased unit activity during convergence. This decrease in firing rate was greater when the monkey converged in downgaze than in upgaze, a finding that corresponds to the observed convergence-associated torsional movements in humans. More recently, dynamic magnetic 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 attachments to the lateral rectus and inferior rectus muscles.

From an evolutionary perspective, it is worth examining whether these torsional movements during convergence simply represent primitive adaptations that have been phylogenetically retained, like the small ocular counterroll which has no known function in humans.17 In the lateral-eyed animal, upgaze corresponds to an intorsional movement of both eyes when the rotation is viewed from the frontal perspective, while downgaze corresponds to an extorsional rotation of both eyes. One could argue that convergence in humans may simply stress the system to a degree that prevents binocular suppression of these primitive rotations. However, recent studies suggest that the frontal binocular visual system has latched on to this primitive torsional bias and exapted it to subserve stereoscopic perception in the pitch plane.50,51 To subserve stereopsis, the oblique muscles have been exapted to torsionally align the eyes with their corresponding visual images in a way that preserves the binocular horizontal disparities that produce stereoscopic perception in different positions of vertical gaze.51 This exaptation serves to minimize the brain's computational load for stereoscopic perception.51

Human cyclovergence is most robust at near fixation, where it plays an active role in stereoscopic vision. If convergence were not linked to cyclovergence, symmetrical convergence on a frontoparallel plane would induce incyclodisparity of the horizontal images in upgaze and excyclodisparity of the horizontal images in downgaze for each eye, solely on the basis of the geometric angle from which each eye views a planar surface. (The opposite cyclodisparity bias occurs for vertical visual landmarks due to projection geometry; however, it is reduced or reversed by the horizontal retinal shear that was described by Helmholtz.40) In convergence, the increased intorsion of the eyes in upgaze and extorsion in downgaze helps to torsionally align the horizontal meridians of the eyes with their respective horizontal visual landmarks, thereby facilitating stereopsis. Since convergence is generally used for downgaze, where near objects are situated, the innervational link between convergence and extorsion presumably serves to set the operational position for stereopsis as slightly in downgaze, where near objects can be held by the arms and illuminated by overhead light.40,41,52 Although the torsional movements associated with convergence are preprogrammed,17 they exhibit remarkable plasticity53 and are enhanced by the depth perception of stereograms,54 demonstrating that they also rely on visual input to more accurately subserve the needs of binocular vision and depth perception. Without these torsional movements, convergence during vertical gaze would limit optimal stereoscopic perception to 1 gaze elevation, requiring repositioning of the head to optimize depth perception of targets at different earth elevations. Thus, this oblique muscle exaptation provides the luxury-optimizing stereopsis for targets at different eye elevations without the necessity of head movements in the pitch plane.

Almost 30 years ago, Blakemore et al32 recorded action potentials from binocular neurons in the cat's visual cortex and measured orientation selectivity during simultaneous binocular stimulation. Certain binocular cells responded specifically to objects tilted in 3-dimensional space toward the cat or away from it.32 Such binocular cells may form at least part of the substrate for sensory cyclofusion in humans. The survival value of stereoscopic spatial orientation explains why cyclofusional movements are so limited in primary gaze and why sensory cyclofusion is so well developed.37,55,56 Sensory cyclofusion without motor cyclofusion is a prerequisite for pitch stereopsis (ie, slant perception). Motor cyclofusion of these torsionally disparate vertical landmarks would induce a misperception 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 landmarks are selectively used in humans to lock in torsional eye position, although the neural feedback loops for this process are unknown. As early as 1861, Nagel35 observed that the rotation of horizontal fusion contours produced cyclovergence, while the rotation of vertical contours produced only a stereoscopic effect.28 Ogle and Ellerbrock37 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. According to Bradshaw and Rogers,57 cyclovergence is not well driven by disparities along vertical meridians even when these are created by a real inclined surface. By inducing cyclodisparity of horizontal lines to the 2 eyes dichoptically, small cyclofusional eye movements can be elicited in humans under experimental conditions.7,20,23,24,37,38,56 The small size of these cyclofusional movements suggests that the human cyclovergence system is equipped to provide a fine-motor modulation to a system that is designed primarily for stability rather than movement.7 The greater stereoscopic value of vertically compared than horizontally tilted images explains why vertically oriented gratings evoke smaller cyclovergence movements than horizontally oriented gratings.23

Humans inhabit a terrestrial environment composed of primarily vertical and horizontal landmarks that serve as reference points for vertical orientation.21,22 In a terrestrial setting, the most prominent horizontal contour is the horizon, which may be the main visual reference for stabilizing the eyes relative to the outside world.21 While cyclodisparities of vertical contours may be caused by slant of the observed objects, cyclodisparities of horizontal contours indicate cyclovergence errors that need correction.20,21 As summarized 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.

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 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 reproducible 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 recruit the oblique muscles to control cyclovergence and thereby assure accurate stereoscopic perception of vertical objects in the pitch plane. While a cyclodisparity of horizontal lines are the driving force for this cyclofusional reflex, stereopsis and vertical visual orientation are its emergent functions.

If a binocular vertical cyclodisparity produces a stereoscopic sensation of pitch, then ocular torsion produced by cyclovertical muscle palsy should produce an abnormal sensation of pitch stereopsis. Not surprisingly, abnormal pitch stereopsis is a common symptom of acquired superior oblique palsy. Lindblom et al59 found that adults with acquired unilateral or bilateral superior oblique palsy perceived the upper pole of a vertical rod as being tilted toward them in the sagittal plane under binocular conditions. This stereoscopic illusion corresponded to the associated extorsion of the paretic eye (Figure 4). Subjects also perceived the unfused image corresponding to the eye with the superior oblique palsy as intorted (ie, tilted in the roll plane) relative to the other image.

As seen in superior oblique palsy, the concept of Panum's space can be extrapolated to torsional eye position. Ocular torsion within the realm of fusion induces an illusory pitch stereopsis of isolated vertical lines, while torsion outside the realm of fusion induces torsional diplopia in the roll plane.5,60,61 Ocular torsion of 5°, as generally occurs with unilateral superior oblique palsy, is not an impediment to fusion, whereas ocular torsion of more than 10°, which accompanies bilateral superior oblique palsy, precludes fusion.6 In unilateral superior oblique palsy, it is often stated that strabismus surgery or prismatic correction to vertically realign the eyes is sufficient to restore cyclofusion, even when the extorsion persists in the palsied eye. However, the persistence of extorsion in one eye is not without perceptual consequence, and it should be remembered that sensory fusion of torsional images can cause vertical objects to be perceived as slanted. Psychophysical experiments by Howard and Kaneko62 have shown that an isolated shear disparity of vertical lines will induce a stereoscopic slant, whereas a cyclodisparity that twists both vertical and horizontal lines will not induce a perceived slant of the visual environment. These experiments would predict that patients with unilateral superior oblique palsy and extorsion of 1 eye would stereoscopically perceive isolated visual landmarks in the sagittal plane as slanted toward them.

Cycloversion, Nonstereoscopic Perception, and the Roll Plane

Unlike cyclovergence, which is remarkably stable and seems to depend primarily on where the eyes are looking, human cycloversion shows both intrasubject and intersubject variation.39 These findings implicate different neural control strategies for cycloversion and cyclovergence.39 One explanation for this disparity is that cycloversion is probably not as important to stereoscopic vision as cyclovergence, which determines stereoscopic volume at any given pitch plane, alters slant perception of vertical objects, and is necessary for stereo constancy.39

Nevertheless, large cycloversional movements of the eyes create a problem for stereoscopic perception. Misslisch et al17 have argued that the superimposition of a primitive cycloversion movement of the eyes (such as an ocular counterroll evoked by a head tilt) on convergence would induce a cyclodisparity and disrupt stereoacuity. The brain strikes a balance between gyroscopic and stereoptic mechanisms by damping the ocular counterroll by approximately 70% in convergence.18 In this way, exaptations of the neural circuitry that steers our cyclovergence and cycloversion movements seem to override our primitive adaptations to promote stereopsis.39,50

While the human oblique muscles function under static conditions to constrain torsional rotation of the eyes, it is not the physiologic role of any muscle to simply constrain movement (check ligaments and muscle pulleys are better suited to this function). To the surprise of many, Tweed et al63 have recently found that the human oblique muscles execute large cycloversional saccades immediately preceding head movements in the roll plane. The 3-dimensional scleral search coil recordings were performed as normal study participants observed a laser spot while their eyes were directed 20° downward. The subjects then made combined eye-head movements to refixate the laser spot as it jumped 20° (from right head tilt and right gaze to left head tilt and left gaze). Eye movement recordings showed that these subjects generated ipsiversive torsional saccades that ranged in size from 11° to 17° and averaged 14.5°. These cycloversional eye movements preceded the head movements by 20 to 60 milliseconds, indicating that these movements were not vestibular in origin. The eyes arrived at the target first and locked on, hanging in space as the head rotated around them (Figure 5). When the head came to a halt, the ocular torsion relative to the head had stabilized near zero, and the eyes were poised for the swiftest possible response to further movement of the target. These torsional eye movements, which occur at the initiation of a head tilt and are not visible on gross inspection, may reveal another exaptation of our torsional control system. The human oblique muscles may have been exapted to generate saccadic torsional eye movements to reestablish roll plane orientation in anticipation of a postural rotation in the roll plane. These anticipatory saccades instantaneously recalibrate torsional eye position to provide a stable visual representation of tilt in the roll (frontal) plane. The evolution of frontally positioned eyes for stereopsis may have created a survival advantage for the grafting of this new torsional control system on top of the ancestral control system that produces the ocular counterroll (Table 1). Similar torsional saccades have not been observed in lateral-eyed animals (although studies involving eye-head or eye-body coordination in animals are extremely difficult to perform).

Reversion From Exaptation to Adaptation

Since ocular torsion within the realm of fusion can produce a stereoscopic tilt in the pitch plane, it seems reasonable to ask whether strabismus or other neurologic disease, which can be associated with a pathologic tilt in the internal representation of the gravitational vertical, could recalibrate prenuclear innervation to the extraocular muscles and produce a torsional deviation of the eyes that conforms to this internal shift. Again, the answer is yes. One of the primitive functions of the human oblique muscles is to rotate the eyes toward the subjective visual vertical; when this internal representation is altered under pathologic conditions, ocular torsion is the inevitable result. In humans, as in lower animals, the central vestibular system uses weighted input from the 2 labyrinths and weighted visual input from the 2 eyes to establish subjective vertical orientation in pitch and roll.64,65 In humans, cycloversion is evoked by visual or graviceptive imbalance in the roll plane,64 whereas cyclovergence is evoked by a visual or graviceptive imbalance in the pitch plane.65 In the roll plane, unilateral loss of otolithic tone secondary to brainstem, cerebellar, or utricular injury causes skew deviation, whereas asymmetrical visual input in humans with congenital strabismus evokes dissociated vertical divergence (Table 1).65 In skew deviation, unequal graviceptive tone from the otoliths produces a pathologic tilt in the internal representation of the visual vertical in the roll plane, which is associated with a corresponding torsional repositioning of both eyes and a vertical divergence of the eyes(Table 1).66 In dissociated vertical divergence, a dorsal light reflex in the roll plane is also associated with visually induced tilt in the subjective visual vertical, and the cycloversional component is ipsidirectional to the patient's perceived visual tilt.67 Since the cycloversional component of dissociated vertical divergence does not accompany the dorsal light reflex in lateral-eyed animals, and it cannot be accounted for by anatomical repositioning of the extraocular muscles, this component of the human dorsal light reflex seems to represent an exaptation to restore vertical orientation during monocular viewing.67 The associated cycloversion movement that occurs when humans fuse vertically disparate images68,69 may indicate that binocular vertical disparity in humans is similarly misregistered by the brain as tilt.70

In the pitch plane, these same primitive adaptations are operative. Donahue and I65 have proposed that primary oblique muscle overaction is associated with a slant of the internal representation of the visual vertical in the pitch plane. A subjective inclination of the superior portion of the visual environment toward the individual would produce a corresponding extorsion of both globes and lead to inferior oblique muscle overaction.65 Conversely, structural neurologic disease within the brain stem or cerebellum would produce the intorsion and superior oblique muscle overaction so commonly seen in children with Chiari malformations, meningomyelocele, or hydrocephalus.65 The alternating skew deviation on lateral gaze with bilateral abducting hypertropia that is associated with craniocervical disease may represent another central vestibular disturbance in the pitch plane.71,72

Under pathological conditions, the oblique muscles still function to keep the eyes in binocular torsional register with the perceived visual environment, and an altered torsional position of the eyes constitutes an ocular motor recalibration to the tilted or slanted internal representation of the visual world that characterizes central vestibular disease. By recognizing that a subjective tilt of the visual environment evokes a corrective torsional repositioning of both eyes, we can begin to place the horse before the cart in understanding congenital strabismus.

CONCLUSIONS

To understand why you really need your oblique muscles, it is necessary to distinguish primitive adaptations, which originally evolved to stabilize laterally placed eyes during body pitch and roll, from exaptations, which subsequently evolved to meet the needs of frontal binocular vision. The human oblique muscles have been exapted to override primitive torsional adaptations with newer mechanisms that subserve stereopsis. These exaptations govern the relative torsional alignment of the eyes in different positions of gaze. Since perception of stereoscopic slant is a function of torsional eye position, the human oblique muscles modulate cyclovergence to establish a stable stereoscopic pitch representation of the visual world. In the roll plane, the human oblique muscles generate a cycloversion movement of the eyes just prior to volitional head movement to lock in a stable visual perception of tilt. These exaptations provide spatial accuracy and temporal continuity to our stereoscopic visual perception of slant and our nonstereoscopic visual perception of tilt. In a larger sense, they furnish us with a multifaceted torsional control system that provides 3-dimensional stability to the visual world and thereby improves fitness.

Exaptations in human oblique muscle function do not completely erase more primitive adaptations. These primitive adaptations produce the small vestigial torsional eye movements that can be measured experimentally by inducing pitch or tilt of the external visual environment. They manifest clinically when congenital strabismus or other central vestibular disease alters our internal representation of the visual vertical. One may conclude that only our primitive adaptations are vestigial; our oblique muscles are not.

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Article Information

Submitted for publication June 7, 2001; final revision received February 12, 2002; accepted February 28, 2002.

This study was supported in part by a grant from Research to Prevent Blindness, Inc, New York, NY.

Corresponding author and reprints: Michael C. Brodsky, MD, Arkansas Children's Hospital, 800 Marshall St, Little Rock, AR 72202.

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