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Chapter 7: Ocular Motor System

Valentin Dragoi, Ph.D., Department of Neurobiology and Anatomy, The UT Medical School at Houston


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7.1 Introduction

The simplicity of the motor systems involved in controlling eye musculature make them ideal for illustrating the mechanisms and principals you have been studying in the preceding material on motor systems. They involve the action of few muscles and of well defined neural circuits.

We use our eyes to monitor our external environment and depend on our ocular motor systems to protect and guide our eyes. The ocular motor systems control eye lid closure, the amount of light that enters the eye, the refractive properties of the eye, and eye movements. The visual system provides afferent input to ocular motor circuits that use visual stimuli to initiate and guide the motor responses. Neuromuscular systems control the muscles within the eye (intraocular muscles); the muscles attached to the eye (extraocular muscles) and the muscles in the eyelid. Ocular motor responses include ocular reflexes and voluntary motor responses to visual and other stimuli. The complexity of the circuitry (the chain or network of neurons) controlling a ocular motor response increases with the level of processing involved in initiating, monitoring, and guiding the response.

In this chapter we will start at the level of reflex responses and move onto more complex voluntary responses in the following lecture. The eye blink reflex is the simplest response and does not require the involvement of cortical structures. In contrast, voluntary eye movements (i.e., visual tracking of a moving object) involve multiple areas of the cerebral cortex as well as basal ganglion, brain stem and cerebellar structures.

7.2 Ocular Reflex Responses

The ocular reflexes are the simplest ocular motor responses. Ocular reflexes compensate for the condition of the cornea and for changes in the visual stimulus. For example, the eye blink reflex protects the cornea from drying out and from contact with foreign objects. The pupillary light reflex compensates for changes in illumination level, whereas the accommodation responses compensate for changes in eye-to-object-viewed distance. Note that reflex responses are initiated by sensory stimuli that activate afferent neurons (e.g., somatosensory stimuli for the eye blink reflex and visual stimuli for the pupillary light reflex and accommodation responses).

In general, ocular reflexes are consensual (i.e., the response is bilateral involving both eyes). Consequently, a light directed in one eye elicits responses, pupillary constriction, in both eyes. In this chapter you will learn of the structures normally involved in performing these ocular responses and the disorders that result from damage to components of neural circuit controlling these responses.

A. The Eye Blink Reflex

Tactile stimulation of the cornea results in an irritating sensation that normally evokes eyelid closure (an eye blink). The response is consensual (i.e., bilateral) - involving automatic eyelid closure at both eyes.

The corneal eye blink reflex neural circuit: This neural circuit (Figure 7.1) is relatively simple, consisting of the

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Figure 7.1
The corneal eye blink reflex is initiated by the free nerve endings in the cornea and involves the trigeminal nerve and ganglion, the spinal trigeminal tract and nucleus, interneurons in the reticular formation, motor neurons in the facial nucleus and nerve, and the orbicularis oculi. As the afferent information from each cornea is distributed bilaterally to facial motor neurons by the reticular formation interneurons, the eye blink response is consensual, that is, both eye lids will close to stimulation of the cornea of either eye.

B. Pupillary Light Reflex

The pupillary light reflex involves adjustments in pupil size with changes in light levels.

The pupillary light reflex allows the eye to adjust the amount of light reaching the retina and protects the photoreceptors from bright lights. The iris contains two sets of smooth muscles that control the size of the pupil (Figure 7.2).

Both muscles act to control the amount of light entering the eye and the depth of field of the eye1.

Normally the sphincter action dominates during the pupillary light reflex.

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Figure 7.2
Iris dilator and sphincter muscles and their actions.

The pupillary light reflex neural circuit: The pathway controlling pupillary light reflex (Figure 7.3) involves the

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Figure 7.3
The pupillary light reflex pathway. The lines ending with an arrow indicate axons terminating in the structure at the tip of the arrow. The lines beginning with a dot indicate axons originating in the structure containing the dot. Bilateral damage to pretectal area neurons (e.g., in neurosyphilis) will produce Argyll-Robertson pupils (non-reactive to light, active during accommodation).

Recall that the optic tract carries visual information from both eyes and the pretectal area projects bilaterally to both Edinger-Westphal nuclei: Consequently, the normal pupillary response to light is consensual. That is, a light directed in one eye results in constriction of the pupils of both eyes.

C. Pupillary Dark Response

The pupils normally dilate (increase in size) when it is dark (i.e., when light is removed). This response involves the relaxation of the iris sphincter and contraction of the iris dilator. The iris dilator is controlled by the sympathetic nervous system.

The pupillary dark reflex neural circuit: The pathway controlling pupil dilation involves the

Axons from the superior cervical ganglion also innervate the face vasculature, sweat and lachrymal glands and the eyelid tarsal muscles. When the superior cervical ganglion or its axons are damaged, a constellation of symptoms, known as Horner's syndrome, result. This syndrome is characterized by miosis (pupil constriction), anhidrosis (loss of sweating), pseudoptosis (mild eyelid droop), enopthalmosis (sunken eye) and flushing of the face.

D. The Accommodation Response

The accommodation response is elicited when the viewer directs his eyes from a distant (greater than 30 ft. away) object to a nearby object (Nolte, Figure 17-40, Pg. 447). The stimulus is an “out-of-focus” image. The accommodation (near point) response is consensual (i.e., it involves the actions of the muscles of both eyes). The accommodation response involves three actions:

Pupil accommodation: The action of the iris sphincter was covered in the section on the pupillary light reflex. During accommodation, pupil constriction utilizes the "pin-hole" effect and increases the depth of focus of the eye by blocking the light scattered by the periphery of the cornea (Nolte, Figure 17-39, Pg. 447). The iris sphincter is innervated by the postganglionic parasympathetic axons (short ciliary nerve fibers) of the ciliary ganglion (Figure 7.3).

Lens accommodation: Lens accommodation increases the curvature of the lens, which increases its refractive (focusing) power. The ciliary muscles are responsible for the lens accommodation response. They control the tension on the zonules, which are attached to the elastic lens capsule at one end and anchored to the ciliary body at the other end (Figure 7.4).

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Figure 7.4
The ciliary muscles, which control the position of the ciliary processes and the tension on the zonule, control the shape of the lens. The ciliary muscles function as a sphincter and when contracted pull the ciliary body toward the lens to decrease tension on the zonules (see Figure 7.5). The decreased tension allows the lens to increase its curvature and refractive (focusing) power. When the ciliary muscle is relaxed, the ciliary body is not pulled toward the lens, and the tension on the zonules is higher. High tension on the zonules pulls radially on the lens capsule and flattens the lens for distance vision. The ciliary muscles are innervated by the postganglionic parasympathetic axons (short ciliary nerve fibers) of the ciliary ganglion

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Figure 7.5
The accommodation response of the lens: comparing the lens shape during near vision (contraction of the ciliary muscle during accommodation) with lens shape during distance vision (relaxation of the ciliary muscle).

Convergence in accommodation: When shifting one's view from a distant object to a nearby object, the eyes converge (are directed nasally) to keep the object's image focused on the foveae of the two eyes. This action involves the contraction of the medial rectus muscles of the two eyes and relaxation of the lateral rectus muscles. The medial rectus attaches to the medial aspect of the eye and its contraction directs the eye nasally (adducts the eye). The medial rectus is innervated by motor neurons in the oculomotor nucleus and nerve.

The accommodation neural circuit: The circuitry of the accommodation response is more complex than that of the pupillary light reflex (Figure 7.6).

The afferent limb of the circuit includes the

Ocular motor control neurons are interposed between the afferent and efferent limbs of this circuit and include the

The efferent limb of this system has two components: the

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Figure 7.6
The accommodation pathway includes the afferent limb, which consists of the entire visual pathway; the higher motor control structures, which includes an area in the visual association cortex and the supraoculomotor area; and the efferent limb, which includes the oculomotor nuclei and ciliary ganglion. The lines ending with an arrow indicate axons terminating in the structure at the tip of the arrow. The lines beginning with a dot indicate axons originating in the structure containing the dot. During accommodation three motor responses occur: convergence (medial rectus contracts to direct the eye nasally), pupil constriction (iris sphincter contracts to decrease the iris aperture) and lens accommodation (ciliary muscles contract to decrease tension on the zonules).

7.3 Clinical Examples

An excellent way to test your knowledge of the material presented thus far is by examining the effects of damage to structures within the ocular motor pathways. The observed motor loss(s) provide clues to the pathway(s) affected; and the muscle(s) and eye affected provide clues to the level of the damage.

Cranial nerve damage: Damage to cranial nerves may result in sensory and motor symptoms. The sensory losses would involve those sensations the cranial nerve normally conveys (e.g., taste from the anterior two thirds of the tongue and somatic sensations from the skin of the ear - if facial nerve is damaged). The motor losses may be severe (i.e., a lower motor neuron loss that produces total paralysis) if the cranial nerve contains all of the motor axons controlling the muscles of the normally innervated area.

The cranial nerves involved in the eye blink response and pupillary response are the optic, oculomotor, trigeminal and facial nerves.

7.4 Clinical Example #1

Symptoms. The patient, who appears with a bloodshot left eye, complains of an inability to close his left eye. When asked to rise his eyebrows, he can only elevate the right eyebrow. When asked to close both eyes, the right eyelid closes but the left eyelid is only partially closed. Touching the right or left cornea with a wisp of cotton elicits the eye blink reflex in the right eye, but not the left eye (Figure 7.7). However, the patient reports he can feel the cotton when it touches either eye. He can smile, whistle and show his teeth, which indicates his lower facial muscles are functioning normally. Physical examination determines that touch, vibration, position and pain sensations are normal over the entire the body and face. There are no other motor symptoms.

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Figure 7.7
Observe the reaction to a wisp of cotton touching the patient's left and right cornea.

Observation: You observe that the patient

You conclude that his left eye's functional loss is

Pathway(s) affected: You conclude that structures in the following motor pathway have been affected

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Figure 7.8
The eye blink pathway involves the trigeminal nerve, spinal trigeminal tract and nucleus, the reticular formation, and the facial motor nucleus and nerve.

Side & Level of damage: As the eye blink loss involves

Conclusion: You conclude that the damage involves

When lower motor neurons are damaged, there is a flaccid paralysis of the muscle normally innervated. The action of the muscle will be weakened or lost depending on the extent of the damage. There will be a weakened or no reflex response and the muscle will be flaccid and may atrophy with time.

The Facial Nerve. Section of the facial nerve on one side will result in paralysis of the muscles of facial expression on the ipsilesional side of the face. There will be an inability to close the denervated eyelid voluntarily and reflexively. The eyelids may have some mobility if the oculomotor innervation to the levator is unaffected.

7.5 Clinical Example #2

Symptoms. The patient complains of a badly infected left eye. When he is asked to close both eyes, both eyelids close. Touching the right cornea with a wisp of cotton elicits the eye blink reflex in the both eyes (Figure 7.9, Right). However, touching the left cornea with a wisp of cotton does not elicit the eye blink reflex in the either eye (Figure 7.9, Left). The patient cannot detect pinpricks to his left forehead. However, he reports that pinpricks to rest of his face are painful. He can blink, wrinkle his brows, smile, and whistle and show his teeth, which indicates his facial muscles are functioning normally. Physical examination determines that touch, vibration, position and pain sensations are normal over the entire the body and over the lower left and right side of his face.

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Figure 7.9
Observe the reaction to a wisp of cotton touching the patient's left and right cornea.

Observation: You observe that the patient

You conclude that his left eye's functional loss is

Pathway(s) affected: You conclude that structures in the following reflex pathway have been affected

Side & Level of damage: As the eye blink loss involves

Conclusion: You conclude that the damage involves

The Trigeminal Nerve. Section of the trigeminal nerve will eliminate somatosensory sensation from the face and the eye blink reflex (e.g., with section of the left trigeminal nerve, light touch of the left cornea will not produce an eye blink in the left or right eye). However, light touch of the right cornea will elicit a bilateral eye blink. The effect of sectioning the trigeminal nerve is to remove the afferent input for the eye blink reflex.

7.6 Clinical Example #3

Symptoms. The patient complains of pain in her left eye. Her left pupil appears dilated and is not reactive to light directed at either the left or right eye (Figure 7.10). The right pupil appears normal in size and reacts to light when it is directed in the right or left eye. Both eyelids can be elevated and lowered and both eyes exhibit normal movement. Touch, vibration, position and pain sensations are normal over the entire the body and face. There are no other motor symptoms.

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Figure 7.10
Observe the reaction of the patient's pupils to light directed in the left or right eye.

Observation: You observe that the patient has

You conclude that his left eye's functional loss is

Pathway(s) affected: You conclude that structures in the following motor pathway have been affected

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Figure 7.11
The pupillary light reflex pathway involves the optic nerve and the oculomotor nerve and nuclei.

Side & Level of damage: As the pupillary light reflex loss

Conclusion: You conclude that the damage

Parasympathetic Innervation of the Eye. Section of the parasympathetic preganglionic (oculomotor nerve) or postganglionic (short ciliary nerve) innervation to one eye will result in a loss (motor) of both the direct and consensual pupillary light responses of the denervated eye. Section of the left short ciliary nerve or a benign lesion in the left ciliary ganglion will result in no direct response to light in the left eye and no consensual response in the left eye when light is directed on the right eye (a.k.a., tonic pupil). When the damage is limited to the ciliary ganglion or the short ciliary nerve, eyelid and ocular mobility are unaffected.

7.7 Clinical Example #4

Symptoms. The patient presents with a left eye characterized by ptosis, lateral strabismus, and dilated pupil. When asked to rise his eyelids, he can only raise the lid of the right eye. When asked to close both eyes, both eyelids close fully. His left pupil does not react to light directly or consensually (Figure 7.12). When asked to look to his right, his left eye moves to a central position, but no further. The right eye is fully mobile. When the patient is asked to look straight ahead, you note his left eye remains directed to the left and depressed. Physical examination determines that touch, vibration, position and pain sensations are normal over the entire the body and face. There are no other motor symptoms.

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Figure 7.12
The patient presents with a left eye characterized by ptosis, lateral strabismus and dilated pupil. Observe the reaction of the patient's pupils to light directed in the left or right eye.

Observation: You observe that the patient

You conclude that his left eye's functional loss is

Pathway(s) affected: You conclude that structures in the following motor pathway have been affected

Side & Level of damage: As the ocular loss involves

Conclusion: You conclude that the damage

The Oculomotor Nerve. Section of the oculomotor nerve produces a non-reactive pupil in the ipsilesional side as well as other symptoms related to oculomotor nerve damage (e.g., ptosis and lateral strabismus). Section of the oculomotor nerve on one side will result in paralysis of the superior levator palpebrae, which normally elevates the eyelid. It will also paralyze the medial, superior & inferior rectus muscles and the inferior oblique, which will allow the lateral rectus to deviate the eye laterally and the superior oblique to depress the eye. The parasympathetic preganglionic axons of the Edinger-Westphal nucleus, which normally travel in the oculomotor nerve, will be cut off from the ciliary ganglion, disrupting the circuit normally used to control the iris sphincter response to light.

7.8 Clinical Example #5

Symptoms. The patient complains of reduced vision in the left eye. Pupil size in both eyes appears normal. However, both pupils do not appear to constrict as rapidly and strongly when light is directed into his left eye (Figure 7.13). That is, compared to the response to light in the left eye, light in the right eye produces a more rapid constriction and smaller pupil in both eyes. Physical examination determines that touch, vibration, position and pain sensations are normal over the entire the body and over the lower left and right side of his face.

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Figure 7.13
Observe the reaction of the patient's pupils to light directed in the left or right eye.

Observation: You observe that the patient's pupils

You conclude that his left eye's functional loss is

Pathway(s) affected: You conclude that structures in the following motor pathway have been affected

Side & Level of damage: As the pupillary light response deficit involves

Conclusion: You conclude that the damage

The Optic Nerve. Partial damage of the retina or optic nerve reduces the afferent component of the pupillary reflex circuit. The reduced afferent input to the pretectal areas is reflected in weakened direct and consensual pupillary reflex responses in both eyes (a.k.a., a relative afferent pupillary defect).

Section of one optic nerve will result in the complete loss of the direct pupillary light reflex but not the consensual reflex of the blinded eye. That is, if the left optic nerve is sectioned, light directed on the left (blind) eye will not elicit a pupillary response in the left eye (direct reflex) or the right eye (consensual response). However, light directed in the right eye will elicit pupillary responses in the right eye and the left (blind) eye. The effect of sectioning one optic nerve is to remove the afferent input for the direct reflex of the blinded eye and the afferent input for the consensual reflex of the normal eye. Section of one optic tract will not eliminate the direct or consensual reflex of either eye as the surviving optic tract contains optic nerve fibers from both eyes. However, the responses to light in both eyes may be weaker because of the reduced afferent input to the ipsilesional pretectal area.

7.9 Clinical Example #6

Symptoms. A patient who is suffering from the late stages of syphilis is sent to you for a neuro-ophthalmological work-up. His vision is normal when corrected for refractive errors. He has normal ocular mobility and his eyelids can be elevated and depressed at will. Examination of his pupillary responses indicates a loss of the pupillary light reflex (no pupil constriction to light in either eye) but normal pupillary accommodation response (pupil constricts when the patient's eyes are directed from a distant object to one nearby).

Observation: You observe that the patient has normal vision but that his pupils

You conclude that his eye's functional loss is

Pathway(s) affected: You conclude that structure(s) in the

Side & Level of damage: As the pupillary response deficit

Conclusion: You conclude that the damage

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Figure 7.14
The accommodation pathway includes the supraoculomotor area, which functions as a "higher-order" motor control stage controlling the motor neurons and parasympathetic neurons (i.e., the Edinger-Westphal neurons) of the oculomotor nucleus. This area was spared by syphilis.

In the Argyll Robertson response, there is an absence of the pupillary light reflex with a normal pupillary accommodation response. The Argyll Robertson response is attributed to bilateral damage to pretectal areas (which control the pupillary light reflex) with sparing of the supraoculomotor area (which controls the pupillary accommodation reflex).

The accommodation response involves many of the structures involved in the pupillary light response and, with the exception of the pretectal area and supraoculomotor area, damage to either pathway will produce common the symptoms. The most common complaint involving the accommodation response is its loss with aging (i.e., presbyopia). Recall that presbyopia most commonly results from structural changes in the lens which impedes the lens accommodation response.

7.10 Summary

This chapter described three types of ocular motor responses (the eye blink, pupillary light and accommodation responses) and reviewed the nature of the responses and the effectors, efferent neurons, higher-order motor control neurons (if any), and afferent neurons normally involved in performing these ocular responses. Table I summarizes these structures and the function(s) of these ocular motor responses. Readers should understand the anatomical basis for disorders that result from damage to components of neural circuit controlling these responses.

Table I
Classification of Consensual Ocular Responses & Their Motor Control Structures
Ocular Responses Function Afferent Input* & Motor Control Structures
Eye Blink Reflex Protects cornea from contact with foreign objects

Free Nerve Endings in cornea that are afferent endings of the Trigeminal Nerve, Ganglion, Root & Spinal Trigeminal Tract*

Spinal Trigeminal Nucleus*

Reticular Formation (bilaterally to)

Facial Motor Nuclei & Facial Nerves

Orbicularis Oculi

Pupillary Light Reflex Decreases pupil size (constriction) – reduces the amount of light that enters the eye.

Retina, Optic Nerve, Chiasm & Tracts and Brachium of Superior Colliculus*

Pretectal Areas of Midbrain (bilaterally to)

Edinger-Westphal Nuclei & Oculomotor Nerves

Ciliary Ganglia & Short Ciliary Nerves

Iris Sphincters

Pupillary Accommodation


Lens Accommodation

Increases depth of focus of eye lens system


Increases refractive power of lens

Visual System* including Visual Association Cortex

Supraoculomotor Nuclei (bilaterally to)

Edinger-Westphal Nuclei & Nerve III

Ciliary Ganglia & Short Ciliary Nerves

Iris Sphincters & Ciliary Muscles

Convergence Eyes directed nasally during accommodation

Visual System* including Visual Association Cortex

Supraoculomotor Nuclei (bilaterally to)

Oculomotor Nuclei

Medial Rectus Muscles

* Afferent structures proving sensory input.

Test Your Knowledge

  • Question 1
  • A
  • B
  • C
  • D
  • E

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve

B. abducens nucleus

C. Edinger-Westphal nucleus

D. pretectal areas

E. supraoculomotor nucleus

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve This answer is INCORRECT.

Optic nerve is incorrect as section of one nerve would not obliterate the consensual response to stimulation of the contralesional eye.

B. abducens nucleus

C. Edinger-Westphal nucleus

D. pretectal areas

E. supraoculomotor nucleus

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve

B. abducens nucleus This answer is INCORRECT.

Abducens nucleus is incorrect as it is not involved in pupillary responses. Its motor neurons innervate the lateral rectus muscle.

C. Edinger-Westphal nucleus

D. pretectal areas

E. supraoculomotor nucleus

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve

B. abducens nucleus

C. Edinger-Westphal nucleus This answer is INCORRECT.

Edinger-Westphal is incorrect as damage to this nucleus would diminish the pupil response both to light and during accommodation.

D. pretectal areas

E. supraoculomotor nucleus

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve

B. abducens nucleus

C. Edinger-Westphal nucleus

D. pretectal areas This answer is CORRECT!

The pretectal area provide bilateral input to the Edinger-Westphal nucleus for the direct and consensual pupillary light response.

E. supraoculomotor nucleus

A patient is capable of pupillary constriction during accommodation but not in response to a light directed to either eye. The lesion is most likely present in the...

A. optic nerve

B. abducens nucleus

C. Edinger-Westphal nucleus

D. pretectal areas

E. supraoculomotor nucleus This answer is INCORRECT.

Supraoculomotor nucleus is incorrect because it is involved in the pupillary accommodation response and not in the pupillary light reflex response.

 

 

 

 

 

 

 

 

 

 

 

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