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Chapter 5
ORBITAL GEOMETRY
ANATOMY OF EXTRAOCULAR MUSCLES

Key Words:  muscle planes, fields of action, primary, secondary and tertiary actions, agonist-antagonist pairs,   Descartes-Sherrington law of reciprocal innervation.
Helpful references: Chapter 9 in Leigh and Zee /  Chapter 5, section 1 in Adler

Outline
V.  Orbital Geometry;   Anatomy, Morphology, and Mechanics of EOM

• Semicircular canals: an ocular gyroscope
   
• Extraocular muscle orientation and actions
  Points of insertion and angles with respect to globe (compare to cat & rabbit)
  Actions- primary, secondary and tertiary
  Conventional and soft pulley models
  Pascal Benzene ring notation
  Diagnosis of noncomitancies - Hess screen, Lancaster test, Superior oblique palsies
   
• Laws of muscle action
  Agonist and antagonist pairs- within eye interaction
  Descartes-Sherrington law of reciprocal innervation
  Force equilibrium  between agonists and antagonists
  Binocular yoking- between eye interaction
  Hering's law of equal innervation
   
• (Outline continues in Chapter 6)

Semicircular canals: an ocular gyroscope
Comparative studies help us to understand the geometry of the orbit, globe and extraocular muscles.  Afoveate eyes mainly served to survey the environment during locomotion.  These eyes are visual gyroscopes that work exclusively with the vestibular canals and their function is to stabilize the image of the world as the animal moves about.  It is helpful to look at the geometry of the vestibular canals to see this point.  There are three pairs of canals (Horizontal, Anterior and Posterior).  These canals lie in three plains that are nearly perpendicular to one another (i.e. orthogonal).  This orthogonality improves their resolution of head motion in 3-D space.  The horizontal canal lies in a plane nearly parallel to the ground.  It is slightly elevated by 30 degrees.  The anterior and posterior canals form a right angle with one another and they lie midway between the sagittal and frontal planes at an angle of 45 degrees.  This orientation is consistent across the animal kingdom, even in fish, birds and reptiles.  The stability of this orientation must have something to do with the mirror symmetry of organs in the head about the midsagittal plane.  In addition, the orientation produces differential pairs on the two sides of the head so that when one canal is optimally stimulated its antagonist is inhibited.  This opponence improves the linearity of the vestibular signal.

 
Extraocular muscle orientation & actions
Consider the orientation of muscles in the eyes.  They too are organized into three planes where each plane contains a muscle pair which acts as agonist and antagonist. The medial and lateral rectus lie in a horizontal plane that is parallel to the floor of the orbit.  The Obliques lie in a plane that forms an angle of about 51 degrees with the midsagittal plane and the vertical recti form a third plane that is nearly perpendicular to the obliques and form an angle of 23 degrees with respect to the medial wall of the orbit.  Thus the three muscle planes are orthogonal and they nearly parallel the vestibular canals.  

Fig 5.2  Muscle plane diagram for the superior rectus and superior oblique.

As you might expect, the orientation of eye muscles varies little across vertebrates.  Rabbits, cats and primates all have eye muscles that have nearly the same orientation in the head, and that orientation is approximately parallel to the orientation of the vestibular canals.  Clearly, the main job of the eye muscles in evolution has been to provide an ocular gyroscope to stabilize the retinal image as we move our head and body during locomotion.  As discussed in the next paragraph, the migration of the line of sight from laterally eyed animals to straight ahead has had little if any influence on the location of the ocular muscles as they insert on the globe.

Next consider the changes that occurred in the orientation of the orbit and ocular globe during evolution.   There appears to be a gradual transition from laterally placed eyes in afoveate animals to forward placed eyes in foveates.  The laterally placed eyes gave the advantage of panoramic vision (360 deg) whereas forward placed eyes causes large overlap of the visual field, a chance for stereopsis, and a sharp view of what's in front of us.  The rabbit has laterally placed eyes with its orbits and globe oriented 90 degrees from the midsaggital plane and the visual axis points midway between the vertical recti and obliques.  (See Fig 5.4 below)  In cat, the globe has migrated forward to align the eyes within 15 degrees of straight ahead.  The vertical recti are nearly in exact alignment with the visual axis and the plane of the obliques nearly forms a 90 degree angle with the visual axis.

Finally in man, the globe is nearly parallel to the midsagittal plane and the visual axis lies midway between the oblique and vertical recti muscle planes. The medial walls of the orbit are parallel to each other and the lateral walls subtend an angle of 90 degrees with one another. Clearly, there is a predominant influence of vestibular orientation rather than visual orientation that guides the orientation of the ocular muscle planes.  The muscles in all animals respond similarly to posture of the head.  However due to differences in the direction of the visual axes, they respond very differently to motion of the retinal image.  Pure vertical upward motion in the cat stimulates a response by the superior rectus.  In man vertical motion stimulates a response by both the inferior oblique and superior rectus.  In rabbit vertical motion stimulates contraction of the superior oblique and superior rectus.  The obliques have opposite actions in primates and rabbits.

There are some interesting species variations on how the muscles fold around one another.  (See Fig 5.6 below.)   Normally the obliques and vertical recti overlap one another.  Sometimes the oblique is above and sometimes underneath the rectus, and sometimes the two muscles are slit and pass through one another.  In man the inferior obliques pass over the inferior rectus and the superior oblique passes under the superior rectus.  However in most mammals the vertical recti lie over the obliques.  In tigers, the recti cut through the obliques, and in lions the superior rectus cuts through the superior oblique but the inferior oblique cuts through the inferior rectus.  This information is also covered in the beginning of chapter 5 in Adler's Physiology of the Eye.

Once we know the geometry of the muscle planes we can easily predict the actions of individual muscles when the eye is in various positions in the orbit.  The actions are referred to as primary, secondary and tertiary.  Primary actions are the main movements caused by the muscle when the visual axis starts in primary gaze.  The primary position of gaze is defined as the position of the eyes in binocular vision when, with the head erect, the object of regard is at infinity and lies at the intersection of the sagittal plane of the head and a horizontal plane passing through the centers of rotation of the two eyes.

The lateral and medial recti have primary actions of abduction and adduction, respectively.  They have no other secondary or tertiary actions from the primary position.  However when the eye is elevated, co-contraction of the lateral recti produces further elevation with a bridle effect.

The inferior and superior recti have primary actions of depression and elevation, respectively.  Due to their oblique insertions on the globe of 23 degrees, they also have secondary actions of excyclo and incyclo rotation, and a tertiary action of adduction.
The inferior and superior obliques also have an oblique insertion on the globe of 51 degrees.  The primary actions of the inferior and superior obliques are excyclo and incyclotorsion, their secondary actions are elevation and depression and their tertiary action is abduction.

Note that the primary, secondary, and tertiary actions of a muscle describe the movement of the eye when the eye starts from the primary position (straight ahead).  With the exception of the horizontal rectus muscles, the directions the eye is pulled by the actions of a muscle (from the primary position) do not correspond to the diagnostic position of gaze in which the eye is placed to test the strength of that muscle.  The diagnostic positions of gaze, also called the cardinal positions of gaze, are determined by aligning the muscle and the optical axis.

The diagnostic gaze of the vertical recti and obliques is the direction where the muscle acts as a pure vertical mover.  Thus the diagnostic gaze (or position) for the obliques is "in" adduction and for the recti in abduction.

Movements of the eye caused by muscle contraction starting in non primary positions can be predicted easily from the muscle planes.  When the visual axis is in a muscle plane that muscle acts as a pure elevator or depressor with the exception of the medial and lateral recti. When the visual axis is perpendicular to the muscle plane the muscles act as pure torters.  For example when the eye is adducted 67 degrees, the vertical recti are pure torters.  Similarly when the eye is abducted 39 degrees the obliques are pure torters.  In intermediate locations the vertical movers also act as adductors and abductors.  The above description is described in Adler's text as the single-action model.  It is useful in interpreting ocular deviations resulting from paresis of one ocular muscle.  The paired antagonist model is also described in Adler's text.

Pascal-Benzene Ring
The Pascal-Benzene ring can be helpful in diagnosing the deviations of the eye when a muscle is paretic.  Distortion-filter tests such as the red lens and Maddox rod are often used to diagnose muscle paresis.  With these tests, perception of direction is opposite to the ocular deviation.  (With projection tests like Lancaster, projection equals the direction of the deviation.)

Fig 5.10  (below) Examples of Paresis measured with the red lens test. A (RLR); B (RMR); C (RIR); D (RSR); E (RSO); F (RIO).

The most common paresis that optometrists see is of the superior oblique.  This is because the fourth cranial nerve has a long and vulnerable pathway.  (The 6th nerve innervation of the lateral rectus is even more vulnerable, but paresis of the lateral rectus is so dramatic that patients automatically go to a neurologist when one occurs.)

The more subtle problems caused by a paretic superior oblique can be discovered by the optometrist.  If the superior oblique is weakened, the patient will have difficulty looking down and in (e.g., looking at the the tip of one's nose).  Since the secondary job of the superior oblique is depression, the affected eye will have a hypertropia.  The vertical deviation is exacerbated if the head is torted towards the same side as the affected eye.

For example, consider the case in which the left superior oblique is weakened.  If the head torts about the visual axis towards the left, the left superior oblique attempts (and fails) to intort and depress the left eye.  The paired muscle in the right eye, the right inferior rectus, extorts and depresses the right eye.  The symptom of a weakened superior oblique is an increased hypertropia when the head is tilted to the side of the paretic eye.  As a result, the patient may unconsciously tilt his/her head to the opposite side to minimize action of the weakened superior oblique.  (See Fig 5.12D below)

This compensating head tilt is known as an ocular torticollis.  (It should be distinguished from an orthopedic torticollis, which is a problem of the neck muscles and joints, not the extraocular muscles.) When the head is tilted to the nonparetic side (ocular torticollis), increased downward torque of the inferior rectus of the paretic eye overcompensates for the secondary action of the inferior oblique (upward torque) and produces a downward deviation of the paretic eye that nulls or corrects for the hyper deviation.  The adaptation permits correction of the vertical deviation with less head turn.  Vertical elevation of paretic SO increases with head tilt to side of affected muscle (positive Bielchowsky sign).  The increased vertical deviation results from an overaction of the superior rectus with upward torque which normally counteracts for the secondary action (depression) of the now paretic superior oblique.  The overaction increases with time indicating that this is an adaptation of the ocular counter-roll reflex which is beneficial in ocular torticollis with the head tilted toward the side of the non-paretic eye but which is counterproductive when the head is tilted to the side of the paretic eye.  The patients can use a variable head tilt to correct the non-comitant vertical deviation as gaze shifts toward and away from the field of action of the superior oblique.

 
Laws of muscle action
Of course no muscle ever acts in isolation.  Movements of the eyes are accomplished by actions of several muscles.  In fact, all six muscles are actively innervated in maintaining the eyeís position in all directions of gaze.  Unlike skeletal muscle, the ocular muscles never rest. They always exert a force on the eye even when itís not moving.  Muscles which facilitate a movement in a particular direction are called agonists while those that oppose the movement are called antagonists.  Each muscle plane contains both an agonists and antagonist.  The direction of the movement determines whether a given muscle is acting as an agonist or antagonist.  During a movement there is an increased innervation of the agonist and decreased innervation of the antagonist.  Sherrington described this reciprocal innervation in 1893.  Descartes-Sherrington's law of reciprocal innervation states that the agonist and antagonist extraocular muscles are reciprocally innervated.  Sherrington demonstrated the reciprocal innervation in a monkey whose III and IV cranial nerves were severed.  Thus only the lateral recti innervated by the 6th cranial nerves could operate.  The monkey could still make conjugate left and right movements of both eyes.  The abducting movement was produced by active innervation of one eye while the adducting movement of the other eye was caused by inhibition of the other lateral rectus.  We shall see that the brainstem contains neurons that orchestrate activation of agonists while they inhibit the antagonist for a given movements of the eyes.

Hering's Law states the the eyes are yoked.  Pairs of muscles in the two eyes that move them in the same direction are called yoked muscles, or synergists.  Conjugate movements are not executed by the same or homologous muscles in the two eyes.  The obliques in one eye are yoked with the vertical recti in the other eye.  The lateral rectus in one eye is yoked with the medial rectus in the other eye.  Typically these yoked muscles are innervated simultaneously to produced conjugate movements of the two eyes.   Disconjugate eye movements are produced by innervating muscles that move the eyes in opposite directions. An example of a conjugate subroutine is the VOR.  Stimulation of the left horizontal canal by a leftward eye movement causes innervation of the 6th nerve on the right half of the brain stem.  Interneurons originating in the 6th nerve cross back to the left half of the brain stem to innervate the third nerve nucleus and cause contraction of the left medial rectus.  Thus yoked rightward movement is orchestrated by a preset innervation linking the right lateral rectus and left medial rectus.  This yoking is adaptable.  For example, when spectacle corrections are worn for anisometropia, one ocular image is magnified more than the other and unequal yoked movements of the eyes are needed to maintain bifoveal fixation.  The eyes learn to make these disconjugate movements (which persist even when one eye is occluded) in less than one hour.  This adjustment is referred to clinically as prism adaptation.  We'll cover this topic later when we discuss vergence eye movements.

Review Questions:
1.  Describe the primary and secondary actions of all six extraocular muscles.
2.  Describe extraocular muscle actions of both eyes during head roll to the right and left.
3.  List the pairs of yoked muscles (e.g., the right superior oblique is paired with the left _____________).

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