Part 2 book “Human neuroanatomy” has contents: Ocular movements and visual reflexes, lower motor neurons and the pyramidal system, the extrapyramidal system and cerebellum, the olfactory and gustatory systems, the limbic system, the hypothalamus, the autonomic nervous system, the cerebral hemispheres, the meninges, ventricular system, and cerebrospinal fluid,… and other contents.
CHAPter 13 Ocular Movements and Visual Reflexes 13.1 OCULAR MOVEMENTS 13.9 VESTIBULAR NYSTAGMUS 13.2 CONJUGATE OCULAR MOVEMENTS 13.10 THE RETICULAR FORMATION AND OCULAR MOVEMENTS 13.3 EXTRAOCULAR MUSCLES 13.11 CONGENITAL NYSTAGMUS 13.4 INNERVATION OF THE EXTRAOCULAR MUSCLES 13.12 OCULAR BOBBING 13.5 ANATOMICAL BASIS OF CONJUGATE OCULAR MOVEMENTS 13.13 EXAMINATION OF THE VESTIBULAR SYSTEM 13.6 MEDIAL LONGITUDINAL FASCICULUS 13.14 VISUAL REFLEXES 13.7 VESTIBULAR CONNECTIONS RELATED TO OCULAR MOVEMENTS FURTHER READING 13.8 INJURY TO THE MEDIAL LONGITUDINAL FASCICULUS 13.1 OCULAR MOVEMENTS often move separately Ocular fixation and coordination of ocular movements take place by about months of age 13.1.1 Primary position of the eyes Normally our eyes look straight ahead and steadily fixate on objects in the visual field This is the primary position (Figs 12.3 and 13.1) of the eyes In this position, the visual axes of the two eyes are parallel and each vertical corneal meridian is parallel to the median plane of the head The primary position is also termed the position of fixation or ocular fixation The position of rest for the eyes exists in sleep when the eyelids are closed In the newborn, the eyes 13.2 CONJUGATE OCULAR MOVEMENTS Moving our eyes, head, and body increases our range of vision Under normal circumstances, both eyes move in unison (yoked together or conjoined) and in the same direction There are several types of such movements, termed conjugate ocular movements: (1) miniature ocular movements, (2) saccades, (3) pursuit movements, and (4) vestibular movements The eyes move in opposite directions, independent of Human Neuroanatomy, Second Edition James R Augustine © 2017 John Wiley & Sons, Inc Published 2017 by John Wiley & Sons, Inc Companion website: www.wiley.com/go/Augustine/HumanNeuroanatomy2e 208 ● ● ● CHAPter 13 each other but with equal magnitude, when both eyes turn medially to a common point such as during convergence of the eyes Such nonconjugate ocular movements are termed vergence movements 13.2.1 Miniature ocular movements Because of a continuous stream of impulses to the extraocular muscles from many sources, the eyes are constantly in motion, making as many as 33 back and forth miniature ocular movements per second These miniature ocular movements occur while we are conscious and have our eyes in the primary position and our eyelids are open We are unaware of these movements in that they are smaller than voluntary ocular movements and occur during efforts to stabilize the eyes and maintain them in the primary position These miniature ocular movements enhance the clarity of our vision The arc minute is a unit of angular measurement that corresponds to one‐sixtieth of a degree Each arc minute is divisible into 60 arc seconds During these miniature ocular movements, the eyes never travel far from their primary position – only about 2–5 minutes of arc on the horizontal or vertical meridian The retinal image of the target remains centered on a few receptors in the fovea where visual acuity is best and relatively uniform Miniature ocular movements encompass several types of movements These include flicks (small, rapid changes in eye position, 1–3 per second, and about minutes of arc), drifts (occurring over an arc of about minutes), and physiological nystagmus (consisting of high‐frequency tremors of the order of 50–100 Hz with an average amplitude of less than minute of arc – 5–30 arc seconds is normal) 13.2.2 Saccades In addition to miniature ocular movements, two other types of voluntary ocular movements are recognized Saccades (scanning or rapid ocular movements) are high‐velocity movements (angular velocity of 400–600° s–1) that direct the fovea from object to object in the shortest possible time Saccades occur when we read or as the eyes move from one point of interest to another in the field of vision While reading, the eyes move from word to word between periods of fixation These periods of fixation may last 200–300 ms The large saccade that changes fixation from the end of one line to the beginning of the next is termed the return sweep Humans make thousands of saccades daily that are seldom larger than 5° and take about 40–50 ms In normal reading, such movements are probably 2° or less and take about 30 ms Hence saccades are fast, brief, and accurate movements brought about by a large burst of activity in the agonistic muscle (lateral rectus), with simultaneous and complete inhibition or silencing in the antagonistic muscle (medial rectus) Another burst of neural activity then steadily fixes the eye in its new position The eye comes to rest at the end Inferior oblique: elevates adducted eyeball Superior rectus: elevates abducted eyeball Medial rectus: adducts eyeball Superior oblique: depresses abducted eyeball Lateral rectus: abducts eyeball Inferior rectus: depresses abducted eyeball Figure 13.1 ● Certain actions of the muscles of the right eye In the center, the eye is in its primary position with its six muscles indicated Left of center the medial rectus adducts the eye The inferior oblique elevates the adducted eye (left and above, the adducted eye is elevated by the inferior oblique) while the superior oblique depresses the adducted eye (left and below) The lateral rectus abducts the eye (to the right of center) while the superior rectus elevates the abducted eye (right and above) The inferior rectus depresses the abducted eye (right and below) (Source: Adapted from Gardner, Gray, and O’Rahilly, 1975.) Ocular Movements and Visual Reflexes of a saccade not by the braking action of the antagonistic muscle but rather due to the viscous drag and elastic forces imposed by the surrounding orbital tissues When larger changes are necessary beyond the normal range of a saccade, movement of the head is required Saccades are rarely repetitive, rapid, and consistent in performance regardless of the demands on them It is possible to alter saccadic amplitude voluntarily but not saccadic velocity The ventral layers of the superior colliculus of the midbrain play an important role in the initiation and speed of saccades and also the selection of saccade targets Areas of the human cerebral cortex thought to be involved in the paths for saccades include the intraparietal cortex, frontal eye fields, and supplementary eye fields Numerous functional imaging studies have shown that human intraparietal cortex is involved in attention and control of eye movements (Grefkes and Fink, 2005) There is an age‐related increase in visually guided saccade latency 13.2.3 Smooth pursuit movements Another type of conjugate ocular movement is the smooth pursuit or tracking movements that occur when there is fixation of the fovea on a moving target This fixation on the fovea throughout the movement ensures that our vision of the moving object remains clear during the movement The amplitude and velocity for such tracking movements depend on the speed of the moving target – up to a rate of 30° s–1 Without the moving visual target, such movements not take place Many of the same cortical areas involved in the paths for saccades (the intraparietal cortex, the frontal eye fields, and the supplementary eye fields) are involved in pursuit movements along with the middle temporal and medial superior temporal areas Apparently, these overlapping areas have separate subregions for the two types of movements There is an age‐related decline in smooth pursuit movements such that eye velocity is lower than the target velocity 13.2.4 Vestibular movements The vestibular system also influences ocular movements Movement of the head is required when larger changes in ocular movements are necessary beyond the size of normal saccades The eyes turn and remain fixed on their target but, as the head moves to the target, the eyes then move in a direction opposite to that of the head Stimulation of vestibular receptors provides input to the vestibular nuclei that signals the velocity of the head needed and provides a burst of impulses causing ocular movements that are opposite to those of the head (thus moving the eyes back to the primary position) The brain stem reflex responsible for these movements is termed the vestibulo‐ocular reflex (VOR) Such movements are termed compensatory ocular movements because they are compensating for the movement of the head and moving the eyes back to the primary position ● ● ● 209 13.3 EXTRAOCULAR MUSCLES Regardless of the type of ocular movement, the extraocular muscles, nerves, and their nuclei, and the internuclear connections among them, all participate in ocular move ments The extraocular eye muscles include the medial, lateral, superior, and inferior recti and the superior and inferior obliques (Figs 13.1 and 13.2) Except for the inferior oblique, all other extraocular muscles arise from the common tendinous ring, a fibrous ring that surrounds the margins of the optic canal The extraocular muscles prevent ocular protrusion, help maintain the primary position of the eyes, and permit conjugate ocular movements to occur Human extraocular muscles contain extrafusal (motor) and intrafusal (spindle) muscle fibers or myocytes The extrafusal myocytes include at least two populations of myocytes and nerve terminals Peripheral myocytes that are small in diameter, red, oxidative, and well suited for sustained contraction or tonus are termed “slow” or tonic myocytes These tonic myocytes receive their innervation from nerves that discharge continuously, are involved in slower movements, and maintain the primary position of the eyes Indeed, extraocular muscles seldom show signs of fatigue in that they work against a constant and relatively light load at all times There are no slow myocytes in the levator palpebrae superioris The inner core of large extraocular myocytes have “fast,” phasic, or twitch myocytes that are nonoxidative in metabolism and better suited for larger, rapid movements This inner core of large extraocular myocytes receives its innervation through large‐diameter nerves that are active for a short time Cholinesterase‐positive “en plaque” endings and “en grappe” endings are on both types of myocytes The “en grappe” endings are somatic motor terminals that are smaller, lighter stained clusters or chains along a single myocyte Sections of human extraocular muscles reveal muscle spindles in the peripheral layers of small‐diameter myocytes near their tendon of origin with about 50 spindles in each extraocular muscle Extraocular muscles are richly innervated skeletal muscles compared with other muscles in the body In spite of this, humans have no conscious perception of eye position Each spindle has 2–10 small‐diameter intrafusal myocytes enclosed in a delicate capsule Nerves enter the capsule and synapse with the intrafusal myocytes Age‐related changes in human extraocular muscles include degeneration, loss of myocytes with muscle mass, and increase of fibrous tissue occurring before middle age and with increasing frequency thereafter These findings probably account for age‐related alterations in ocular movements, contraction and relaxation phenomena, excursions, ptosis, limitation of eyelid elevation, and convergence insufficiency All extraocular muscles participate in all ocular movements, maintaining smooth, coordinated ocular movements at all times Under normal circumstances, no extraocular muscle acts alone, nor is any extraocular muscle allowed to act fully hiding the cornea Movement in any direction is under the influence of the antagonist extraocular muscles that actively participate in ending a saccade by serving as a brake In some rare individuals, the eyes can be 210 ● ● ● CHAPter 13 (A) Superior oblique Superior rectus Medial rectus Lateral rectus Tendon of levator palpebrae superioris (B) Superior oblique Tendon of levator palpebrae superioris Lateral rectus Superior rectus Inferior oblique Medial rectus Inferior rectus voluntarily “turned up” with open lids and the corneas hidden from view The eyelids remain closed in sleep and while blinking – an involuntary reflex involving brief (0.13–0.2 s) eyelid closure that does not interrupt vision because the duration of the retinal after‐image exceeds that of the act of blinking In young infants, the rate of eye blinking is low, about eight blinks per minute, but this steadily increases over time to an adult rate of 15–20 blinks per minute Bilateral eyelid closure takes place in the corneal reflex (described in Chapter 8), on sudden exposure to intense illumination, the dazzle reflex, by an unexpected and threatening object that moves into the visual field near the eyes, the menace reflex, or by corneal irritants such as tobacco smoke Application of a local anesthetic to the cornea does not interrupt blinking as it does in the congenitally blind and in those who have lost their sight after birth Figure 13.1 illustrates actions of the extraocular muscles Because of the complexity of the interactions among the extraocular muscles, it is best to examine them in isolation Figure 13.2 ● (A) View from above of the muscles of the right eye Only the tendon of origin remains following resection of the levator palpebrae superioris muscle (B) The muscles of the right eye as seen from the lateral aspect Only the tendon of origin of the levator remains following its resection and removal of the middle of the lateral rectus (Source: Adapted from Gardner, Gray, and O’Rahilly, 1975.) 13.4 INNERVATION OF THE EXTRAOCULAR MUSCLES The six extraocular muscles and the levator of the upper eyelid (levator palpebrae superioris) receive their innervation by three cranial nerves: the oculomotor, trochlear, and abducent The extraocular muscles receive a constant barrage of nerve impulses even when the eyes are in the primary position Impulses provided to the extraocular muscles allow the eyes to remain in the primary position or to move in any direction of gaze Ocular movements take place by increase in activity in one set of muscles (the agonists) and a simultaneous decrease in activity in the antagonistic muscles The eyeball moves if the agonist contracts, if the antagonist relaxes, or if both vary their activity together Therefore, in the control of ocular movements, activity by the antagonists is as significant as activity of the agonists The abducent nerve [VI], or sixth cranial nerve, innervates the lateral rectus The designation LR6 indicates the Ocular Movements and Visual Reflexes lateral rectus innervation The trochlear nerve [IV], or fourth cranial nerve, innervates the superior oblique The designation SO4 indicates the superior oblique innervation The remaining extraocular muscles and the levator palpebrae superioris receive their innervation through the oculomotor nerve [III], the third cranial nerve, for which the designation R3 indicates the pattern of innervation If an extraocular muscle or its nerve is injured, certain signs will appear First, there will be limitation of ocular movement in the direction of action of the injured muscle Second, the patient visualizes two images that separated maximally when attempting to use the injured muscle The resulting condition, called diplopia or double vision, results because of a disruption in parallelism of the visual axes The images are likely to be horizontal (side‐by‐side) or vertical (one over the other), depending on which ocular muscle, nerve, or nucleus is injured 13.4.1 Abducent nucleus and nerve The abducent nerve [VI] supplies the lateral rectus muscle (Figs 13.1 and 13.2) Its nuclear origin, the abducent nucleus, is in the lower pons, lateral to the medial longitudinal fasciculus (MLF), and beneath the facial colliculus on the floor of the fourth ventricle (Fig. 13.3) The abducent axons leave the nucleus and cross the medial lemniscus and pontocerebellar fibers lying near the descending corticospinal fibers as they spread throughout the basilar pons (Fig. 13.3) These intra‐axial relations of the abducent fibers are clinically significant Abducent axons emerge from the brain stem caudal to their nuclear level, at the pontomedullary junction where they collectively form the abducent nerve Individual abducent cell bodies participate in all types of ocular movements, none of which are under exclusive control of a special subset of abducent somata ● ● ● 211 uninjured eye Injury to the abducent nuclei or the abducent nerves will cause a bilateral internal (convergent) strabismus with paralysis of lateral movement of each eye and both eyes drawn to the nose Often this is due to abducent involvement in or near the ventral pontine surface where both nerves leave the brain stem In one series of abducent injuries, the cause was uncertain in 30% of the instances, due to head trauma in 17%, had a vascular cause in 17%, or was due to a tumor in 15% of those examined Other common causes of abducent injury include increased intracranial pressure, infections, and diabetes 13.4.2 Trochlear nucleus and nerve The trochlear nerve [IV] innervates the superior oblique muscle (Fig. 13.2) Its cell bodies of origin are in the trochlear nucleus embedded in the dorsal border of the medial longitudinal fasciculus in the upper pons at the level of the trochlear decussation (Fig. 13.4) The rostral pole of the trochlear nucleus overlaps the caudal pole of the oculomotor nucleus Fibers of the trochlear nerve originate in the trochlear nucleus, travel dorsolaterally around the lateral edge of the periaqueductal gray, and decussate at the rostral end of the superior medullary velum before emerging from the brain stem contralateral to their origin and caudal to the inferior colliculus as the trochlear nerve [IV] The human trochlear nerve has about 1200 fibers ranging in diameter from to 19 µm Upon emerging from the brain stem, the trochlear nerve passes near the cerebral peduncles and then travels to the orbit As they course in the brain stem from their origin to their emergence, trochlear fibers are unrelated to any intra‐axial structures The trochlear nerve is slender, has a long intracranial course, and is the only cranial nerve that o riginates from the dorsal brain stem surface The trochlear nerve is the only cranial nerve all of whose fibers decussate before leaving the brain stem Thus, the left trochlear nucleus supplies the right superior oblique muscle Injury to the abducent nerve The abducent nerve is frequently injured and has a long intracranial course in which it comes near many other structures Thus, in addition to lateral rectus paralysis, other neurological signs are necessary to localize abducent injury Isolated abducent injury is likely to be the only manifestation of a disease process for a considerable period With unilateral abducent or lateral rectus injury, a patient will be unable to abduct the eye on the injured side (Fig. 13.3) Because of the unopposed medial rectus muscle, the eye on the injured side turns towards the nose, a condition called unilateral internal (convergent) strabismus Double vision with images side‐by‐side, called horizontal diplopia, results when attempting to look laterally Weakness of one lateral rectus muscle leads to a lack of parallelism in the visual axis of both eyes Since the injured lateral rectus is not working properly, the paralyzed eye will not function in conjunction with the contralateral Injury to the trochlear nerve Unilateral injury to the trochlear nerve causes limitation of movement of that eye and a vertical diplopia evident to the patient as two images, one over the other (not side‐by‐side as is found with abducent or oculomotor injury) Those with unilateral trochlear injury often complain of difficulty in reading or going down stairs Such injury is demonstrable if the patient looks downwards when there is adduction of the injured eye To compensate for a unilateral trochlear injury, some patients adopt a compensatory head tilt (Fig. 13.4B) With a right superior oblique paresis, the head may tilt to the left, the face to the right, and the chin down (Fig. 13.4B) In such instances, old photographs and a careful history may reveal a long‐standing trochlear injury If the oculomotor nerve is injured and only the abducent and trochlear nerves are intact, the eye is deviated laterally, not laterally and downwards, even though the superior 212 ● ● ● CHAPter 13 (A) Medial Abducent longitudinal nucleus fasciculus Trigeminal spinal nucleus Facial nucleus Facial root fibers Trigeminal spinal tract Abducent root fibers traversing medial lemniscus Abducent root fibers Basilar pons (corticopontine and corticospinal fibers) (B) Downward gaze (C) Right lateral gaze (D) Left lateral gaze (note midposition of left eye) (E) Upward gaze Right Left Figure 13.3 ● (A) A transverse section of the lower pons showing the abducent and facial nuclei, their fibers and their relation to other structures at this level (B–E) The effects on ocular movements of a unilateral left abducent injury Ocular movements are normal except for abduction of the left eye on left lateral gaze (D) The pupils are equal and reactive to light during all movements (Source: Adapted from Spillane, 1975.) oblique is unopposed by the paralyzed inferior oblique and superior rectus In patients with unilateral oculomotor and abducent injury, sparing only the superior oblique innervation, the eye remains in its primary position Superior oblique contraction (alone or in combination with the inferior rectus) does not cause rotation of the vertical corneal meridian (called ocular intorsion) Therefore, the function of the superior oblique is likely that of ocular stabilization, working with the inferior oblique and the superior and inferior recti in producing vertical ocular movements Because trochlear nerve fibers decussate at upper pontine levels before emerging from the brain stem, an injury here often damages both trochlear nerves In 90% of the cases of vertical diplopia, the trochlear nerve is involved The trochlear nerve is less commonly subject to injury than the abducent or oculomotor nerves The list of causes of trochlear nerve paralysis is extensive, including trauma (automobile or motorcycle accident with orbital, frontal, or oblique blows to the head), vascular disease and diabetes with small vessel disease in the peripheral part of the nerve, and tumors Bilateral trochlear nerve injury likely results from severe injury to the head in which the patient loses consciousness and experiences coma for some time The diplopia is usually permanent The most likely site of bilateral fourth nerve injury is the superior medullary velum where the nerves decussate and the velum is thin, such that decussating trochlear fibers are easily detached Ocular Movements and Visual Reflexes (A) ● ● ● 213 Trochlear decussation Lateral lemniscus Superior cerebellar peduncle Medial lemniscus Trochlear nerve Trochlear nucleus Medial longitudinal fasciculus Corticopontine and corticospinal fibers (B) Figure 13.4 ● (A) A transverse section of the upper pons at the level of the trochlear decussation The trochlear nuclei lie rostral to this level but are in view here to emphasize the trochlear fibers leaving the brain stem (indicated by dashed lines) Figure 13.5 illustrates the effects of a unilateral trochlear nerve injury on ocular movements (B) A patient with a unilateral right trochlear nerve injury may manifest a compensatory tilt of the head to the left to reduce the vertical diplopia caused by a unilateral trochlear nerve lesion 13.4.3 Oculomotor nucleus and nerve The oculomotor nerve [III], innervating the remainder (R3) of the extraocular muscles, has its cells of origin in the oculomotor nucleus at the superior collicular level of the midbrain (Fig. 13.5) About 5 mm in length, the oculomotor nucleus extends to the caudal three‐fourths of the superior colliculus Throughout its length, it is dorsal and medial to the medial longitudinal fasciculus but ventral to the aqueduct (Fig. 13.5) At their caudal extent, the oculomotor nuclei fuse and overlap with the rostral part of the trochlear nuclei Various patterns of localization are identifiable in the oculomotor nucleus In the baboon, and presumably in humans, the inferior oblique, inferior rectus, medial rectus, and levator palpebrae superioris muscles receive their innervation from neurons in the ipsilateral oculomotor nucleus whereas the superior rectus receives fibers from neurons in the contralateral oculomotor nucleus Functional neuronal groups in the baboon oculomotor nucleus intermingle with each other and not remain segregated into distinct subnuclei From the oculomotor nucleus, axons arise and cross the medial part of the red nucleus and also the substantia nigra and cerebral crus (Fig. 13.5) These fibers then emerge from the interpeduncular fossa (Fig. 13.5) Once outside the brain stem, each nerve passes between a posterior cerebral and a superior cerebellar artery and then continues in the interpeduncular cistern of the subarachnoid space In course, the oculomotor nerve is on the lateral aspect of the posterior communicating artery traversing the cavernous sinus before it enters the orbital cavity A significant number of ganglionic cells are scattered or clustered in the rootlets of the human oculomotor nerve In addition, afferent fibers with neuronal cell bodies in the trigeminal ganglia are identifiable in the oculomotor nerve in humans On entering the orbit in the lower part of the superior orbital fissure, the oculomotor nerve divides into a superior branch that innervates the superior rectus and the levator palpebrae superioris and an inferior branch that travels to innervate the inferior rectus, medial rectus, and inferior oblique Because of this method of branching, injuries that involve one branch while sparing the other often occur Injury to the oculomotor nerve Unilateral injury to the oculomotor nerve leads to ptosis, abduction of the eye, limitation of movement, diplopia, and pupillary dilatation (Fig. 13.5) Ptosis [Greek: fall], caused by weakness or paralysis of the levator palpebrae superioris, exists if the lid covers more than half of the cornea, including complete closure of the palpebral fissure A mild or partial ptosis with the upper lid covering one‐third or less of the cornea may result from injury to the tarsal or palpebral muscle (of Müller) in the upper eyelid or with 214 ● ● ● CHAPter 13 (A) Aqueduct Superior colliculus Oculomotor nucleus Medial lemniscus Medial longitudinal fasciculus Red nucleus Oculomotor root Substantia nigra Cerebral crus Interpeduncular fossa (B) Eyes straight ahead, right ptosis (C) (D) Both eyes right–right pupil enlarged (E) Eyes upward–right eye remains in midposition, right pupil enlarged Eyes left–right eye remains in midposition, right pupil enlarged (F) Eyes downward–right eye remains in midposition, right pupil enlarged Right Left Figure 13.5 ● (A) A transverse section of the upper midbrain at the level of the oculomotor nucleus and the emerging oculomotor fibers The relation of these fibers to the medial longitudinal fasciculus, red nucleus, and the medial part of the cerebral crus is significant (B–F) Effect on ocular movements and pupillary size of a unilateral right oculomotor nerve injury There is a complete ptosis in (B) In (C–F), the examiner’s finger helps to overcome the ptosis There is a dilated right pupil in (C–F) and intact movement of the right lateral rectus in (D) In (D–F), the right eye is fixed and will not move up (D), medially (E), or down (F) (Source: Adapted from Spillane, 1975.) injury to the innervation of this muscle The tarsal muscle is smooth muscle that has a sympathetic innervation and elevates the lid for approximately 2 mm After injury to both oculomotor nuclei or to both nerves, loss of all ocular movements and the upper eyelids results, with double ptosis Abduction of the eye f ollowing unilateral oculomotor injury is likely due to the unopposed action of the lateral rectus causing external strabismus and the inability to turn that eye medially The abducted eye is turned outwards but not outwards and downwards even though the superior oblique is unopposed by the paralyzed inferior oblique (and perhaps the superior rectus) Pupillary dilatation may result from injury to the preganglionic parasympathetic fibers in the oculomotor nerve These autonomic (pupillomotor) fibers arise from neurons in the accessory oculomotor (Edinger–Westphal) nucleus, a compact neuronal mass on either side of the median plane through the rostral third of the oculomotor nucleus These preganglionic parasympathetic neurons are smaller than oculomotor neurons Each neuronal mass is composed of rostral and caudal parts With an expanding intracranial mass and compression or distortion of the oculomotor nerve, the ipsilateral pupil is frequently dilated, a condition called paralytic mydriasis, without any detectable impairment of the extraocular muscles In one series, most oculomotor nerve injuries were of uncertain origin, 20.7% were vascular in nature, 16% caused by trauma, 13.8% due to aneurysms, and 12% resulted from tumors In the same study, 48.3% of those with signs of oculomotor injury recovered Ocular Movements and Visual Reflexes 13.5 ANATOMICAL BASIS OF CONJUGATE OCULAR MOVEMENTS Under normal conditions, ocular movements in the horizontal plane are dominant over those in other planes in primates In all horizontal movements, it appears that the lateral rectus leads the way and determines the direction of movement As the right eye turns laterally in a horizontal plane, the left eye turns medially Movements of both eyes in a given direction and in the same plane are termed conjugate ocular movements During such movements, the eyes move together (yoked, paired, or joined) as their muscles work in unison with the ipsilateral lateral rectus and the contralateral medial rectus contracting simultaneously as their opposing muscles relax Since motor neurons innervating the lateral rectus are in the lower pons and those innervating the medial rectus are in the upper midbrain, there must be a connection 215 between these nuclear groups if they are to function in concert with one another Abducent neurons supply the ipsilateral lateral rectus Adjoining the inferior aspect of the abducent nucleus (Fig. 13.6) is the crescent‐shaped para‐abducent nucleus Fibers arise from the para‐abducent nucleus, immediately decussate, and as internuclear fibers ascend in the contralateral medial longitudinal fasciculus (Fig. 13.6) to synapse with medial rectus neuronal cell bodies in the oculomotor nucleus The anatomical basis for horizontal conjugate ocular movements involving the simultaneous contraction of the ipsilateral lateral rectus and the contralateral medial rectus depends on these connections Connections exist, allowing the opposing (antagonistic) muscles to relax as the agonist muscles contract Abducent neurons use acetylcholine as their neurotransmitter whereas Medial rectus muscle Lateral rectus muscle Abducent nerve ● ● ● Oculomotor nerve Oculomotor nucleus Trochlear nucleus Medial longitudinal fasciculus Abducent nucleus Vestibular nuclei: Superior Lateral Medial Inferior Figure 13.6 ● Connections between the vestibular nuclei of the medulla, the abducent nuclei of the lower pons, and the trochlear and oculomotor nuclei of the midbrain that underlie horizontal ocular movements from vestibular stimulation (Source: Adapted from Calhoun and Crosby, 1965.) 216 ● ● ● CHAPter 13 the neurons of the para‐abducent nucleus use glutamate and aspartate as neurotransmitters In addition to these cranial nerve ocular motor nuclei, there are premotor excitatory burst neurons that reside rostral to the abducent nucleus, inhibitory burst neurons that reside caudal to the abducent nucleus, and omnipause neurons near the median raphé at the level of the abducent nucleus All three of these neuronal groups (excitatory, inhibitory, and omnipause) and their connections with abducent neurons are essential for horizontal ocular movements Collectively, these three neuronal groups form a physiological entity termed the paramedian pontine reticular formation (PPRF) Perhaps a better term for this group of neurons could be one that recognizes their anatomical relationship to named reticular nuclei in the human rostral medulla and pons in addition to their function 13.6 MEDIAL LONGITUDINAL FASCICULUS The medial longitudinal fasciculus (MLF) is a prominent bundle of fibers in the brain stem that participates in coordinating activity of several neuronal populations This well‐ circumscribed bundle is near the median plane and beneath the periaqueductal gray (Fig. 13.5) The oculomotor nucleus indents the MLF dorsally and medially at the superior collicular level (Fig. 13.5) The trochlear nucleus indents the MLF at upper pons levels (Fig. 13.4) In the lower pons, the MLF is on the medial aspect of the abducent nucleus (Fig. 13.3) Therefore, these three nuclear groups, related to ocular movements, form a column from the superior colliculus to the lower pons and all adjoin the medial longitudinal fasciculus There is a large burst of activity in the agonistic muscle (lateral recti), with simultaneous and complete inhibition in the ipsilateral antagonistic muscle (medial recti) This occurs because there are fibers connecting neurons innervating the lateral rectus of one eye and the neurons innervating the medial rectus of the other eye as a basis for horizontal conjugate ocular movements These fibers form the internuclear component of the medial longitudinal fasciculus (Fig. 13.6) The trigeminal motor, facial, and hypoglossal nuclei and also the nucleus ambiguus have internuclear fibers interconnecting them through the medial longitudinal fasciculus as well These internuclear fibers permit coordinated speech, chewing, and swallowing Connections also exist in the medial longitudinal fasciculus that permit opening and closing of the eyelids while allowing the vestibular nuclei to influence ocular motor nuclei 13.7 VESTIBULAR CONNECTIONS and OCULAR MOVEMENTS In addition to ocular movements in the horizontal plane induced by stimulation of the abducent nerves and nuclei and the medial longitudinal fasciculus, stimulation of many other parts of the nervous system such as the pontine reticular formation, vestibular receptors, nerves, and nuclei, the cerebellum, and the cerebral cortex often result in ocular movements in the horizontal plane Indeed, the vestibular system probably influences ocular movements in all directions of gaze 13.7.1 Horizontal ocular movements Receptors in this path are the vestibular hair cells on the ampullary crest in the lateral semicircular duct Their primary neurons, in the vestibular ganglia, have peripheral processes that innervate these receptors and central processes that pass to the vestibular nuclei (Fig. 13.6) to synapse with secondary neurons The secondary vestibular neurons at medullary levels (the medial, rostral one‐third of the inferior, and the caudal two‐thirds of the lateral vestibular nuclei) participate in this path for horizontal ocular movements Axons of these secondary neurons proceed to the median plane, decussate and ascend in the contralateral medial longitudinal fasciculus (Fig. 13.6) These secondary fibers synapse with lateral rectus motor neurons in the abducent nucleus and with neurons in the para‐abducent nucleus Physiologically, the vestibular nuclear complex influences the contralateral abducent nucleus that innervates the lateral rectus muscle Such connections between these ocular motor nuclei occur through the medial longitudinal fasciculus and are the same connections as those that underlie horizontal conjugate ocular movements A secondary relay system for reciprocal inhibition connects the vestibular nuclei with the ipsilateral abducent and para‐abducent nuclei whose fibers innervate the contralateral oculomotor nucleus It is by way of this secondary relay system in the medial longitudinal fasciculus (Fig. 13.6) that impulses for the inhibition of antagonistic muscles influence these muscles to relax as the agonist muscles contract, permitting smooth, coordinated, conjugate ocular movements By maintaining fixation despite movements of the body and head, the vestibulo‐ocular reflex minimizes motion of an image on the retina as movements of the head occur (If the reader rapidly shakes their head from side‐to‐side while reading these words, the words remain stationary and in focus.) Movements of the head increase activity in the already tonically active vestibular nerves This increased neuronal activity relays to the ocular motor nuclei The connections underlying the vestibulo‐ocular reflex in the horizontal plane are the same as those that underlie horizontal conjugate ocular movements Ocular position at any moment is the result of a balance of impulses from vestibular receptors and nuclei on one side of the brain stem versus impulses coming to the contralateral structures 13.7.2 Doll’s ocular movements Compensatory ocular movements that occur with changes in position of the head are under the influence of vestibular stimuli without influence from visual stimuli Turning the ... Human Neuroanatomy, Second Edition James R Augustine © 20 17 John Wiley & Sons, Inc Published 20 17 by John Wiley & Sons, Inc Companion website: www.wiley.com/go/Augustine/HumanNeuroanatomy2e 22 8 ... opening the eyes Br J Ophthalmol 20 :25 7 29 5 Henn V, Cohen B (19 72) Eye muscle motor neurons with different functional characteristics Brain Res 45:561–568 ● ● ● 22 5 Henn V, Cohen B (1976) Coding... nucleus contains a dorsal part (MGd), a ventral part (MGmc), and a medial part (MGm) The ventral part, also termed the principal or parvocellular part, is the largest part of the MG occupying