VS 117
April 7, 1998
V. Lam

Announcements:
_ Handout #7 passed out
_ Quiz next week on Chapters 5, 7, 8, 9
_ Chapter 12 & 14 on Fixation Eye Movement and Saccades will be discussed next week

Homework from Chapter 22
_ Purpose: to link Maddox classification and clinical case analysis technique (graphical analysis) that we will be using in our clinic courses.
_ The width of the zone of clear and single binocular vision equals the sum the various components of vergence predicted by the Maddox hierarchy.
_ The phoria line is derived by connecting the distance phoria (8) and the near phoria (13B). This line evaluates tonic and accommodative vergence. The convergence range is represented to right of the phoria line. The divergence range is represented to the left of the phoria line. The reciprocal of the slope of the phoria line equals the calculated AC/A ratio.
_ Plot the distance examinatino results, using the bottom axis scale. For near, use the top axis.
_ Tests 9, 10, and 11 are for distance. Tests 16 A& B, 17 A & B, and 19 are for near test results.
_ Blur (9) at distance is a test that stimulates the limit of disparity driven convergence. When they are about to see double most patients cheat a little. They start accommodating to extend their range of convergence by using accommodative convergence. The patient will say, "I still see a single target, but it’s getting blurry." At this point, they have run out of fusional vergence and now are using accommodative vergence. This is called the blur point. To extend the divergence range, a patient can relax accommodation, just before he doubles, to relax some accommodative vergence. At far, there is no accommodation to relax since target is already at infinity. Thus, there is no divergence blur point at far. They just double. This is called the break point. At near, 2.5D of accommodation is already being stimulated so that the divergence range can be extended at near by allowing accommodation to relax and you get a blur point at near.
_ Base out and Base in limits of the zone of clear single binocular vision are not exactly parallel to phoria line. In most cases, the BI side (on the left) is parallel to the phoria line. But the BO side (on the right) tends to fan to the right. Why? If only fusional vergence was available, BO limit would be parallel to phoria line. But additional convergence results from proximal vergence as a stimulus gets closer and closer. This causes the BO limit to fan the zone out to the right. An estimate of proximal vergence can be obtained by seeing how much the zone of binocular vision widens.
_ In the zone of clear, single binocular vision, any combination of lens or prism described by the zone is what the eye can respond to by using the Maddox classification. When fusional, accommodative, and tonic vergence are combined together, they are within the range that this binocular system can respond to.
_ The width of the zone indicates the quality of the binocular system. People with abnormal binocular vision have very narrow zones and fusion ranges. The amount they can converge and diverge from the phoria line may be a very tiny amount. Often this results from an uncorrected vertical phoria.
_ Top of zone is determined by the monocular amplitude of accommodation.
_ Zone will predict limits of relative accommodation. Positive and negative relative accommodation is stimulated by putting minus and plus lenses in front of the two eyes (binocular viewing) until clear vision or fusion is no longer possible.
_ The width of the zone is related to fusional vergence (divergence to the left and convergence to the right). Tonic vergence is the starting point. Fusional vergence is from phoria to limits. Zone limits from phoria point are called fusional vergence.
_ In clinic, we start at the demand point (a single point in real space). Zone limits from demand point are called relative vergence.

CHAPTER 5

There are various interpretations as to what the main actions of the EOMs are, in particular, the obliques. Most see IO and SO as cyclomovers and torters. Others see their primary action is elevation and depression, respectively. Professor Schor does not care what is considered their primary action. Just know what actions are made possible by the obliques.

Table from Adler’s Physiology of the Eye
MUSCLE PRIMARY ACTION SECONDARY ACTION TERTIARY ACTION
Medial Rectus Adduction
Lateral Rectus Abduction
Inferior Rectus Depression Excycloduction (Extortion) Adduction
Superior Rectus Elevation Incycloduction (Intortion) Adduction
Inferior Oblique Excycloduction (Extortion) Elevation Abduction
Superior Oblique Incycloduction (Intortion) Depression Abduction

Think of the eye as sitting inside 3 muscle planes. When the visual axis is aligned with a particular muscle plane (e.g. B below) and those muscles contract, the eyes look vertically. When the eye is pointed perpendicular to the muscle plane and those muscles act, the eye torters.

Fig 5.3 Extraocular muscle planes:
A) Midsaggital plane
B) Plane of vertical rectus muscles
C) Plane of oblique muscles
Note that horizontal rectus muscles (medial
and lateral rectus) lie in a horizontal plane
parallel to the floor of the orbit.

B above is the muscle plane of the vertical recti. If the eye is ABducted 23_, the vertical recti act as pure elevators or depressors. If the eye is turned in perpendicular to muscle plane B toward the nose, then the vertical recti act as pure torters. So the actions of the muscle really depend on where the visual axis is pointing relative to the muscle plane.
Similarly, if the eye is aligned with plane C, pointed 51 degrees toward the nose, then the obliques will act as pure elevators or depressors. But if the eye is pointed outward slightly perpendicular to the oblique muscle plane, then the obliques act as torters.
Just remember, when the eye is pointed parallel to the muscle plane, the muscles mainly act vertically. When the eye is pointed perpendicular to the muscle plane, the muscles act as torters. In between, various combinations of vertical and torsional eye movements are obtained.

How to apply this information clinically?

Eye muscle paresis can be evaluated by putting a red lens or Maddox rod over one eye, and shining a pen light at the patient’s face. The eye without the red lens or Maddox rod will see the pen light as a bright spot. The eye with the red lens or Maddox rod will see a red spot or red streak, respectively. The eye behind the red lens or Maddox rod is going to deviate. The image of the red spot or streak is opposite to the direction that the eye is deviated because the red image is not formed on the fovea. For example, if the eye is deviated up, the image of the target will be imaged above fovea. The image will appear down, opposite to the direction the eye is pointing.

Fig 5.11 Illustration of Maddox Rod percept produced by paresis of left superior oblique.

Question: Is red lens always placed over the weaker eye?
For primary deviations, the red lens is usually put over the weaker eye.
For secondary deviations, the red lens is put over the stronger eye. When the weaker eye tries to fixate, the deviation actually become bigger. The weaker eye has to use more innervation to fixate than does the non-paretic eye. Hering’s law causes all that extra innervation to overstimulate the agonist in the non-fixating non-paretic eye. This causes the deviation to be exaggerated.
Usually, start first with the red lens over the weaker eye to measure the primary deviation. Then place the red lens over the non-paretic eye to see if the deviation increases (secondary deviation). Note that in the figure above, the Maddox rod is placed over the stronger (non-paretic) eye and is measuring the secondary deviation.

Diagram from Cogan’s Book of Classical Neurology
Shine pen light. Eye without red lens is seeing the clear white light. Eye looking through red lens is seeing red light. Grid seen is patient’s view of what they are reporting to you. The grid represents the nine cardinal positions of gaze. The primary position is in the middle looking straight ahead. Secondary positions are vertical or lateral from primary. Tertiary position are in combinations of the vertical and lateral positions.

3_ 2_ 3_
2_ 1_ 2_
3_ 2_ 3_

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

A. Red lens is placed over the right eye (RE). Left eye (LE) has no lens. Shine light on patient’s face and ask patient to look over to the right. LE points to the right. RE cannot move past straight ahead. RE should be pointing to the right. Instead, it is in from where it should be and looking straight ahead. RE sees the red image in the direction it should be looking, over to the right.
Which EOM would prevent the RE from looking temporalward? Right LR. When the patient look to the left, he sees the red and white spot superimposed. As he looks farther to the right, the more separated the red and white images become. Eventually, he will have double vision over to the right.
Damage to which nerve could lead to this condition? ipsilateral abducens (CN VI)

B. Patient is looking to the left. RE cannot look to the left. Double vision is seen over to the left.
Which muscle in the RE is preventing it from looking to the left? Right MR. Which nerve could be damaged? CN III.

C. This person is trying to look down and to the right. RE cannot look down and to the right.
What muscle in the RE is responsible for looking down and to the right? When the eye is ABducted, IR depresses the eye.
What innervates the IR? CN III

D. RE attempts to look up and to the right, but cannot. RE sees the red image elevated because it cannot move the eye up.
What muscle moves the eye up and right? SR. Think of the muscle plane. When the eye is turned out, visual axis is parallel to that muscle plane. Thus, vertical recti act as elevators or depressors. When eye turns inward, obliques are acting as true vertical movers.
When look up, clear light is below red light. This tells you that when look up, eye behind red lens is hypo, since the image is seen as high. Projection is opposite to the deviation because the deviating eye is not foveating the light shining at the eye. So its image is off the fovea. Since foveas correspond, diplopia results.

E. Patient is looking left and down. RE cannot look down when adducted. This is the muscle plane of the obliques. Thus, the obliques are the primary movers for vertical movement.
Which oblique is responsible for turning eye down when ABducted? SO which is innervated by the contralateral trochlear nerve (CN IV) on the left side of the head.

F. Looking up and to the left. RE cannot look up and to the left because the IO is not working. Patient can fuse when direction of gaze is to the right. But when RE is turned left, it sees double in up gaze and more singly in down gaze.
This pattern of muscle paresis is called non-commitancy. The deviation varies with direction of gaze.

Note that the pathways of the CN IV and CN VI are the longest and most tortuous of the cranial nerves. It is common for head trauma to result in a SO (trochlear) or LR (abducens) paralysis (palsy).

Two most of the most common problems patients encounter with trauma:
1. Abducens palsy
This paralyzes the LR and makes them esotropic. The affected eye cannot turn out; it is parked in all the time. They can look medially with that eye, but not temporally. Optometrists generally do not see these patients. They run right to the neurologist because it is such a severe problem.
2. SO palsy
Optometrists see this more often. It results from damage to CN IV. The key symptom is they cannot look down and in at the tip of their nose with the affected eye.

Fig 5.12 Illustration of variations of vertical deviation in LSO palsy with:
A (primary gaze); B (right gaze and left gaze); C (rightward down and up gaze); and D (head tilt to the right and left).

A. Left eye is elevated even in primary gaze. The toughest thing for the patient to do is to turn the eye in and down.

C. RE is unaffected; it can look down and out. But the affected LE cannot look down and in. However, the LE does not do so badly when looking upward and to the right.

D. Patients like to tilt head off to side opposite of the deviating eye in order to eliminate the vertical tropia and see singly. So if left eye has SO palsy, the patient turn his/er head over to the right, allowing the eyes to fuse. This tends to make the eyes level. When tip head to same side of deviation, it exaggerated the vertical deviation and the lower eye is hyper.

Normally, one of the problems with paralysis of the left SO is the eye is not only elevated, but it is extorted as well. No matter what one calls the primary action of the obliques, the main action of the obliques is to the tort the eyes. It does this more than any other ocular muscle. Vertical recti don’t tort the eyes nearly as much as the obliques do.
One of the main actions of the SO is to intort the eye. So if the SO is paretic, the eye rolls out (exorts). Patients like to roll their head opposite to the side of the turned eye, making the eyes more level (ocular torticollis). When the head rolls from one side to the other, the eyes normally try to stay vertical even while the head rolls by torting. This is called ocular counterroll.
This makes sense for rabbits whose eyes point out to the side. If the rabbit is looking at the horizon on each side, and the rabbit rolls its head and wants to keep looking at the horizon, it counterrolls the eyes to keep the eyes level. For us, it is the same as when we pitch our heads back and forth. We want to keep our visual axis level. The vertical counter-roll is called the Doll’s head reflex. Our eyes tend to stay level when we rock our head back and forth. The equivalent reflex for rabbits is to torsional counter-roll. When we evolved, our eyes moved straight ahead, but the torsional counter-roll reflex stayed with us. When the head rolls side to side, eyes still counterroll like a vestigial reflex that made sense when our visual axis was pointed to the side.

Why do we get counter-roll when we roll our heads?
_ It has to do with VOR and Otoliths.
_ Otoliths.
a. These are earstones in the middle ear made of calcium carbonate.
b. When the head is tip to the side, the otoliths tend to tip and pull little hair cells over. The hair cells are gravity sensors that indicate when
the head is upright and when it is turned.
c. Otoliths are sensors of head position mainly, but of acceleration as well.
d. Two kinds of otoliths: 1. utricle which detects head roll, and 2. sacculus which detects vertical motion.

Counter-roll is not very large. It is about 1/10 the amount of head rotation. If the head is rotated 60_, eyes will only counterroll 6_. It really does not make your eyes vertical again.

What muscle is going to counterroll our eyes?
For example, if the head is rotated to the left, what muscle in LE is going to turn the eye back upright? SO will incyclotort the LE by turning it in and pulling eye down. IO will turn RE out to line things up and pull the eye up.

Since there is vertical imbalance caused by the secondary action of the obliques when we tip our head, are we still fusing? We would not be fusing if only the obliques acted on counter-roll. However, we have vertical recti which correct for the secondary vertical action of the obliques. When the head is tipped to the left, the left SO intorts and pulls the eye down and SR counteracts secondary action of SO and realigns the eye. SR pulls eye up while the SO is pulling eye down. The right IO extorts and pulls eye up. So the IR pulls eye back down into alignment.

Ocular counter-roll has three components:
1. Head roll
2. Obliques tort the eyes to correct vertical orientation with torsion, but they also create vertical misalignment.
3. Vertical recti realign eyes and correct for errors induced by the secondary action of the obliques.

Why do patients with trochlear palsy like to tilt their heads?
Ex: LSO palsy.
If the heads tilts to the left (paretic side), the nonfunctional LSO tries to intort eye down. At the same time, LSR starts to pull eye up anticipating that it will counteract the downward pull of the oblique. But the LSO cannot pull the eye down. So when patient rolls head to the left to side of paresis, the deviation is exaggerated. This is called a Postive Bielchowsky sign. It makes the LE go even higher than it already was. The vertical rectus is trying to compensate for a muscle that is no longer working. Normally when head tips to the left, SO would have pulled the eye down while it intorted. But in this case the SO does not work. So the eye is not being pulled down at all. SR does not know this and it pulls the eye up the way it would normally correct the downward pull of the oblique.
What patients learn to do is to exaggerate vertical rectus motion. When head is tilted away from weak eye, IO of the weak eye extorts the eye. Normally, IR pulls against IO to cancel out its secondary vertical effects. But a SO palsy patient learns to exert extra effort by the IR so that it pulls the hypertropic eye and align the eyes vertically. By tilting the head to the left, the IR is used to align the eyes vertically. Overaction of IR pulls eye down so that they are aligned.

Tip head to same side of lesion => exaggerate strabismus
Tip head to opposite side of lesion => minimize strabismus

Stimulation of neck muscles, canals, and utricles causes eye muscles to change their posture. Variable amounts of head tilt are used to stimulate more or less IR activity to keep eyes level.

Picture of girl with RSO palsy.
She likes to carry head to left, which is the side opposite to the palsy. When she tips head to right, RE is much higher. The right corneal reflex is lower than the left. High left corneal reflex because right eye is elevated. When she tilts to the left, the eyes are level and the reflexes are the same. When the eyes are not level, the reflexes can be 20D off. Some of these verticals can even get up to about 35-40 D =~20_ when head tips.

Consequences:
exaggerate IR when tip head to bad side => get rid of hyper
exaggerate SR when tip head to good side => make hyper worse
Adaptation helps when tip head away from deviation
Adaptation worse when tip head toward deviation

It is helpful to tip the head to align the eyes. But if the head is tipped the wrong way, the mechanism of exaggerated vertical recti activity will misalign the eyes.

Bielchowsky Head Tilt Phenomenon
_ change in vertical deviation with head tilt; better on one side and worse on other
_ Positive Bielchowsky sign - vertical elevation of paretic SO increases with head tilt to side of affected muscle

Ocular torticollis
_ when patient reduces vertical strabismus by tilting head to side opposite of deviation in order to have fusion
_ head induced neck turn; can straighten head

Orthopedic torticollis
_ stiff neck; hard to straighten head out
_ not to be confused with ocular torticollis, in which the head can induce a neck turn and the head can be straightened out

SO palsy can be subtle. It does not have to be a strabismus. It can just be a phoria. Patient may not be aware they have a SO palsy. SO palsies are detected when the phoria is measured in different cardinal positions of gaze.

Chapter 7
Cranial nerves are called the final common pathway. EOMs are always moved via those nerves independent of the type of movement, whether it is a saccade, pursuit, OKN, VOR, convergence, divergence. Prior to that in the brainstem, there are specialized regions which control various types of eye movements. For example, vertical gaze movements are controlled by a region above the third nerve nucleus called the riMLF. . Horizontal (lateral gaze) eye movements and pursuits are controlled in the pons region near the abducens nucleus. Convergence eye movements are controlled by near-response cells in vicinity dorsal and lateral to the third nerve nucleus.

Fig 7.1, Table 7.1, and Fig 7.2 (below) Locations of cranial nerves III, IV, & VI, and their nuclei.

Medulla Oblongata Pons Mesencephalon (midbrain)
VIII (vestibular) VI (abducens) III (oculomotor), IV (trochlear)

Chapter 8
At the bottom of the hierarchy of oculomotor control are the muscles, which perform the orbital mechanics. The level above the muscles are the motor neurons which make up the final common pathway and take orders from the specialized centers controlling movement via the III, IV, and VI nerve nuclei in the brainstem. The brainstem finalizes or orchestrates vertical and horizontal eye movements, how fast a saccade is, the velocity of a pursuit, and direction of vergence eye movements. The brainstem follows the orders from the cortex and colliculus, which have regions that determine the direction to move the eyes and how fast to get them to a specific location and distance. Initial velocity is controlled by pre-motor neuron in cortex superior colliculus and brainstem.

Fig 8.1 Hierarchy of Oculomotor Control. Note that Pre-motor neurons operate in Cartesian Coordinates, Motor Neurons operate in Canal Coordinates, and Ocular Muscles operate in Canal Coordinates. (See Chapter 9 for more details)

Chapter 9

Cranial nuclei III, IV, and VI, which send axons via the cranial nerves to musculature, receive instructions from the pre-motor nuclei. The premotor nuclei control horizontal and vertical and disjunctive, and fast and slow eye movements. The interneurons that run the length of the brainstem connecting the premotor nuclei to the specific motor cranial nuclei III, IV, and VI are collectively called the Medial Longitudinal Fasciculus (MLF).

Fig 9.1 Location of Motor and Premotor Nuclei. Note the location of the Medial Longitudinal Fasciculus (MLF) relative to nuclei.

Oculomotor nucleus III
_ controls the ipsilateral MR, IO, IR and the contralateral SR
_ controls accommodation and pupillary constriction in Edinger Westphal which is really part of the third nerve complex

Abducens nucleus VI
_ sends information to both sides of the brainstem
_ innervates ipsilateral LR
_ sends over interneuron to innervate contralateral MR
_ stimulation of one nucleus on one side causes conjugate pulling of eye to same side by activating ipsilateral LR and contralateral MR
_ dual function: 1. lateral gaze center 2. final pathway for LR on ipsilateral side

Note: The two superiors, SR and SO, in an eye are controlled by the opposite side of the brain.

Figure 9.10 Various lesions (ophthalmoplegia) and resulting symptoms. Bars above eyes indicate approximate range of motion. 1) Oculomotor Ophthalmoplegia 2) Abducens palsy 3) Unilateral INO (InterNuclear Ophthalmoplegia) 4) One-and-a-half syndrome 5) Foville’s Syndrome (Posterior INO)

1. Oculomotor Ophthalmoplegia a.k.a. Complete Ophthalmolplegia
_ ophthalmoplegia => total paretic eye
_ total blockage of CN III
_ In the eye which is innervated by a lesion oculomotor nucleus III, only LR, SO, and SR (innervated by contralateral oculomotor nucleus) is working.
_ Typical signs of affected eye: 1. droopy eyelid 2. dilated pupil because Edinger-Westphal lies very close to the CN III which controls ipsilateral pupil and accommodation

2. Abducens Palsy
_ break in connection between CN VI and ipsilateral LR
_ does not affect interneuron going to opposite side
_ effect is RE cannot ABduct, resulting in a little esotropia

3. Unilateral InterNuclear Ophthalmoplegia (INO) a.k.a. Anterior INO
_ only one interneuron from abducens nucleus to contralateral oculomotor nucleus is affected
_ lesion is blocking interneuron from VI nerve nucleus to contralateral MR
_ result: selective loss of MR, adduction of contralateral eye is affected

4. One-and-a-Half Syndrome
_ caused by lesion of abducens and both interneurons
_ affect both MR and ipsilateral LR
_ LR on contralateral side still works
_ ipsilateral eye cannot move horizontally, contralateral eye can move temporally

5. Posterior INO a.k.a. Foville’s Syndrome
_ lateral gaze palsy
_ unilateral lesion at or near abducens nucleus and blocks its projections
_ knocks out one whole lateral gaze center
_ Symptoms: can’t direct either eye to side of lesion
_ cannot adduct contralateral eye and cannot abduct ipsilateral eye
_ indicative of an aneurysm, tumor, or multiple sclerosis

The rest are not shown in the diagram
6. Parinaud’s Syndrome
_ vertical gaze paralysis
_ lesion occurs around superior colliculus in RiMLF (rostral interstitial medial longitudinal fasciculus) which controls vertical saccades, pursuits, etc. Tumor here will affect up and/or down gaze depending on location of tumor.
_ lesion very near region that controls convergence and divergence of eyes

7. Lesion caudal to III
_ cause esotropia
_ failure to adduct while normal vergence ability is retained
_ cannot adduct either eye while attempting conjugate lateral gaze => lateral gaze palsy
_ but can converge both eyes easily to near stimulus due to different pre-motor center of neural control than lateral gaze
_ VOR might work

8. Pseudo-ophthalamoplegia
_ patients cannot move their eyes voluntarily, but can involuntarily
_ shake head -> counter-roll
_ but cannot track object due to separate paths for voluntary and involuntary eye movement

VOR
_ shortest path of all oculomotor reflexes
_ only needs 3 synapses to get to muscle of eye 1. one is in bipolar cell right below hair cell 2. vestibular nucleus 3. in third nerve nucleus
_ takes 10 msec to generate
_ shortest latency of all oculomotor behavior
_ generally affected last; if affected, CN 8 is usually disrupted

Possible causes of muscle problems:
1. Muscle lesion
This is very rare. It usually only occurs due to trauma, e.g. car accidents with glass. CN III and VI are likely to be damaged with trauma.
2. Cranial nerve nucleus affected
Ex: If CN 3 nucleus is affected, all eye movements, like pursuit, saccade, VOR, are affected equally.
3. Lesions at higher level
Specific tasks are impaired. Generally, higher lesions are more indicative of sensory problems.

Recent onset is not a good sign. It is usually associated with trauma. Other symptoms include vertigo, nausea, and disorientation.