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J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

Journal ofNeurology, Neurosurgery, and Psychiatry, 1978, 41, 1084-1091

Reflex vertical gaze and the medial longitudinal fasciculus L. R. JENKYN, G. MARGOLIS, AND A. G. REEVES From the David Prosser Neurology Research Laboratory, Division of Neurology, Department of Medicine, Dartmouth-Hitchcock Medical Center, and the Department of Pathology, Dartmouth Medical School, Hanover, New Hampshire, USA

S U M MARRY Extraocular movements were investigated in a patient with bilateral vascular lesions of the medial longitudinal fasciculus. The patient showed voluntary and reflex horizontal gaze consistent with his lesion, but had absent reflex vertical gaze. Voluntary vertical gaze was present. Necropsy was performed, and the findings suggest that the medial longitudinal fasciculi in the convey impulses for reflex vertical gaze, but are not required for voluntary vertical gaze. by guest. Protected copyright.

Lesions of the medial longitudinal fasciculus Keane, 1975). A mechanism for the move- (MLF) produce characteristic neuro-ophthalmo- ments seen in internuclear ophthalmoplegia has logical findings. Bilateral lesions are most common been postulated by Pola and Robinson (1976), and in demyelinating processes but are also observed recently confirmed by electro-oculographic analysis with occlusive vascular disease and neoplasm of 25 patients (Kirkham and Katsarkas, 1977). (Smith and Cogan, 1959; Christoff et al., 1960; Unilateral hot or cold caloric stimulation of the Cogan, 1970; Gonyea, 1974). With complete semicircular canals results in reflex conjugate bilateral involvement, there is paralysis of adduc- horizontal gaze (Bender, 1959; Shanzer and tion of both with in the abducting Bender, 1959). The reflex response, also known as eye. Vertical nystagmus is usually present on the slow component of nystagmus, is thought to upgaze, and convergence may or may not be pre- originate in the hair cells of the horizontal semi- served. Skew deviation is rarely observed (Smith circular canals and to follow a path to the contra- and Cogan, 1959). In less complete lesions, there lateral paramedian pontine via may be only paresis of adduction with nystagmus the of the side stimulated. This of both eyes in the direction of gaze (Christoff area of the reticular formation is thought to be et al., 1960). Unilateral lesions are caused more the source of integration of both voluntary and commonly by occlusive vascular disease than by reflex conjugate horizontal eye movements demyelinating processes (Cogan et al., 1950; Fine (Bender and Shanzer, 1964; Cohen, 1971; Sharpe and MacGlashan, 1956; Harrington et al., 1966; et al., 1974). With the subject in the supine posi- DeMyer, 1966). tion, unilateral cold stimulation results in reflex Kupfer and Cogan, 1966; Ross and http://jnnp.bmj.com/ The paresis or paralysis of adduction is seen gaze toward the side irrigated, while warm stimula- ipsilateral to the side of the lesion. Abduction tion directs gaze to the opposite side. The cerebral nystagmus is usually present contralateral to the hemispheres are thought to generate a checking or and vertical nystagmus occurs frequently. Con- fast component in the direction opposite to the is preserved. Skew deviation is common slow component that determines the direction of with the elevated eye usually on the side of the the specified nystagmus-that is, nystagmus to the lesion (Smith and Cogan, 1959; Cogan, 1970; left means fast component to the left (Bender, of the lesion. Vertical gaze is usually intact, 1955; Pasik et al., 1960). While some authors cite side on September 24, 2021 the usefulness of double simultaneous caloric This study was supported in part by the Hitchcock Foundation. irrigation in eliciting reflex vertical gaze, we have Address for reprint requests: Dr Lawrence R. Jenkyn, David Prosser found few reports investigating the neural connec- Neurology Research Laboratory, Division of Neurology, Department tions of this mechanism in man (Bender, 1959, of Medicine, Dartmouth-Hitchcock Medical Center, Hanover, New Hampshire 03755, USA. 1960; Shanzer and Bender, 1959; Shanzer, 1964; Accepted 27 June 1978 Shanzer et al., 1964). 1084 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

Reflex vertical gaze and the medial longitudinal fasciculus 1085 In primates, including man, voluntary vertical tion in the carotid . Cerebrospinal fluid gaze is thought to be mediated in the pretectal study revealed protein of 1.12 g/l and glucose of region of the (Bender and Shanzer, 1960; 8.2 mmol/l with all other parameters within Christoff et al., 1962; Shanzer et al., 1964). Volun- normal limits. EEG and scan were normal. tary upgaze is thought to require an intact pre- tectum and (Bender, 1959; NEURO-OPHTHALMOLOGICAL FINDINGS (Fig. 1) Christoff et al., 1962; Pasik et al., 1969a, b), while At rest a skew deviation was present with the left intact structures dorsomedial to the red nuclei are eye 3 mm above the right. Attempts to converge considered necessary for voluntary downgaze after instruction without fixating on a visual target (Bender, 1959; Christoff et al., 1962; Jacobs et al., yielded no eye movements. With tracking of a 1973; Cogan, 1974; Halmagyi et al., 1978). Recent visual target, 2 mm of adduction of the right eye studies in monkeys have confirmed that bilateral and 1 mm of adduction of the left eye were seen. lesions of the MLF eliminate reflex vertical eye An incomplete bilateral MLF syndrome was movements and impair in extremes of present. On voluntary gaze to the right, the right vertical gaze while not affecting voluntary vertical eye abducted 7 mm with nystagmus to the right, (King et al., 1976; Evinger et al., 1977). while the left eye came to the midline without We report a case of bilateral MLF involvement nystagmus. On left lateral gaze, the left eye and impaired reflex vertical gaze with preserved abducted 7 mm with nystagmus to the left, while voluntary vertical gaze which suggest that the the right eye adducted 2 mm past the midline pathway mediating reflex vertical gaze in man includes the medial longitudinal fasciculi. by guest. Protected copyright. 3rr- 2rnm mm Case report (~ <

bilaterally, and dysarthria with slight deviation of http://jnnp.bmj.com/ the to the left. abnormalities OCULOCEPHALIC STIMULATION are described below. He was able to move all '2D~ extremities to command. Paratonia (resistance to 7mm 4mm movements in all directions) was present diffusely, Right: ice water irrigation Bilaterol ice water irrigation and there was a slight drift with pronation of his ~2mm 7mm right upper extremity. Biceps and triceps reflexes <:ED

were absent in the left leg, and the left plantar CALORIC STIMULATION on September 24, 2021 response was flexor. Sucking, forced biting, and Fig. 1 Schematic presentation of neuro- rooting reflexes were present. Abnormal laboratory ophthalmological findings. A large arrow indicates the values were blood glucose of 19.4 mmol/l and direction of active checking. A small arrow indicates blood urea nitrogen of 10 mmol/l. An old septal the direction of minimal intermittent checking. myocardial infarct was detected on electro- Absence of arrow indicates no checking. No cardiography. Skull radiography showed calcifica- measurement indicates no change from midposition. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

1086 L. R. Jenkyn, G. Margolis, and A. G. Reeves without nystagmus. Vertical tracking of an object dilatation. There was pulmonary congestion and resulted in 2 mm upgaze bilaterally with discon- oedema. Atherosclerosis was severe in the aorta jugate nystagmus upwards, and in 7 mm downgaze and moderate in the coronary arteries. The in the right eye and 5 mm downgaze in the left cerebral circulation exhibited mild atherosclerosis eye without nystagmus. without significant narrowing. Optokinetic responses were elicited by use of an The brain showed a 2 mm cystic infarct in the optokinetic drum while the patient was alert. right at the junction of the Optokinetic nystagmus was seen in the right eye, medial and lateral portions. The peduncle medial greater on movement of the stimulus from left to to this zone was palpably softened. In the rostral right than on right to left. In the left eye, there pons, a vertically oriented zone of softening in- was full abduction with the stimulus moving to volved the on the left side from the ven- the patient's left and absent adduction with it tricular surface to the pars basalis. At this point, moving to the right and no nystagmus in either it forked into a Y that extended diagonally across direction. Vertical presentation of the optokinetic into the pars basalis of the contralateral side (Fig. stimulus produced no change in the eyes from 2). The lesion extended caudally 5 mm from the midposition. uninvolved left fourth . The remainder of Horizontal oculocephalic reflex evaluation the was normal. There was also a 30 mm showed only abduction without nystagmus infarct of the left frontal operculum. There was bilaterally. no involvement of the midbrain tectum, teg- Vertical oculocephalic testing revealed a 2 mm mentum, or periaqueductal region. The mamillary deviation of the eyes upward when the chin was bodies appeared normal, and there was no atrophy by guest. Protected copyright. flexed toward the chest. Frenzel glasses were not of the . The showed used, and visual fixation was not controlled with mild generalised atrophy, with moderate dilatation this manoeuvre. With brisk extension of the head of the . the eyes remained in midposition. Microscopic analysis of the lesion in the mid- With the head raised 30 degrees above the pons showed a malacic zone in the left tegmentum horizontal, caloric irrigation was performed with involving the anatomical regions formerly 60 ml of ice water both unilaterally and bilaterally occupied by the medial longitudinal fasciculus, and hot tap water bilaterally, with five minutes and the dorsal, ventral, and superior tegmental between irrigations. Cold stimulation on the right nuclei (Fig. 3, top). The lesion extended to the elicited 7 mm abduction of the right eye without pars basalis of the pons where it crossed the mid- nystagmus and no adduction or nystagmus of the line. The cystic area was partially occupied by left eye. Cold stimulation on the left elicited 7 mm abduction of the left eye with depressed, inter- mittent checking and 2 mm adduction of the right eye with active checking. Double simultaneous ice water stimulation resulted in a 4 mm depression of the right eye with a variable nystagmus some- times to the right and sometimes vertically, and no depression or nystagmus of the left eye. Double simultaneous hot stimulation resulted in no re- sponse from the midposition in either eye. Upward and outward deviation of both eyes on forced http://jnnp.bmj.com/ closure of the lids (Bell's phenomenon) was observed.

COURSE The patient developed gangrene of the left lower extremity, and died two months later with no change in his neurological status. on September 24, 2021

PATHOLOGY Fig. 2 Transverse gross section through rostral pons Gross findings included a recent focal infarct of showing destruction of left medial longitudinal the fasciculus and underlying tegmentum, now evident myocardial septum and an old extensive as a sharply defined cystic zone. No gross alterations antero- and posteroseptal infarct. The heart was of the right medial longitudinal fasciculus are enlarged with left ventricular hypertrophy and recognisable. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

Reflex vertical gaze and the medial longitudinal fasciculus 1087 foamy macrophages and remnants of blood vessels. MLF. There was no reflex upgaze in either eye and There was a diffuse astroglial reaction in the minimal reflex downgaze on the side of the in- surrounding tissues. Throughout the right medial completely involved MLF during double simul- longitudinal fasciculus there was a scattered loss taneous caloric stimulation. The presence of upgaze of myelinated fibres producing a moth-eaten ap- on oculocephalic testing suggests either that the pearance (Fig. 3, bottom). There were also patient was fixating visually during the head flexion scattered, swollen, degenerating axons spread manoeuvre (which obscured the reflex component), throughout the fasciculus. In the surrounding or that the bilateral hot caloric stimulation was not tissues, there was an astroglial reaction involving sufficient to elicit the response. It must be con- the dorsal and superior tegmental nuclei. The re- sidered that the pathway for reflex upgaze may mainder of the brainstem, including the pretectum, differ from that of reflex downgaze. The post- was normal. mortem findings, and the presence of a bilateral MLF syndrome response on caloric stimulation of Discussion each side, imply that the vestibular connections to the paramedian pontine reticular formation were The patient showed signs of diffuse bilateral cere- intact bilaterally. There was complete destruction bral dysfunction and bilateral involvement of the of the paramedian pontine reticular formation by guest. Protected copyright.

V. Fig. 3 Top: transverse microscopic section through rostral pons. The absence :-:. . of parenchyma on the left demarcates the cystic lesion which lha-s effaced the * **'. left medial longitudinal fasciculus. At this low magnification, the right medial longitudinal fasciculus appears approximately normal, except for a few vacuolar zones (Luxol fast blue- haematoxylin eosin, original magnification X45). Bottom: detail of enclosed area from top of figure showing subtle structural lesions iwhich are compatible with functional defects in right medial

longitudinal fasciculus. These consist of http://jnnp.bmj.com/ proliferation of aFtrocytes (A), vacuoles indicating loss of individual myelinated fibres (B), and swollen degenerating axons (C) (original magnification X250). on September 24, 2021 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

1088 L. R. Jenkyn, G. Margolis, and A. G. Reeves only in the rostral pons on the left as well as of reticular formation before turning cephalad to the left MLF, while the right paramedian pontine enter the oculomotor and trochlear nuclei reticular formation was not involved at all, and (Christoff, 1974). This conclusion was based on the the right MLF only partially so. This suggests that absence of vertical gaze observed in three patients the absence of reflex vertical gaze in the left eye with infiltrating of the pons which did not may have been caused by reticular formation in- extend into the midbrain, and four patients with volvement as well as MLF destruction, while im- focal infarctions of the which paired but detectable reflex downgaze of the right extended across the midline. The pathology re- eye was a function of the intact reticular forma- ported in the "locked-in" syndrome demonstrates tion on the right or only partial involvement of preserved voluntary vertical gaze in cases with the right MLF. Despite these hypothetical objec- bilateral destruction of the caudal paramedian tions, it seems that bilateral lesions in the MLF pontine reticular formation (Halsey et al., 1967; were the major factor contributing to impairment Kemper and Romanul, 1967; Chase et al., 1968; of reflex vertical eye movements in this patient. Nordgren et al., 1971; Hawkes, 1974). No reports A recent report of seven cases of the "locked- could be found describing vertical eye movements in" syndrome described one patient with bilateral in patients with bilateral destruction of the rostral reflex downgaze on double simultaneous ice water paramedian pontine reticular formation. The caloric stimulation. Postmortem findings showed above observations suggest that cortical innerva- bilaterally intact medial longitudinal fasciculi, tion of vertical eye movements in man is mediated while the basis pontis and both paramedian reticu- by structures caudal to the midbrain in the rostral

lar formations were destroyed. The author does pons, and this is supported by the experimental by guest. Protected copyright. not comment on the basis for the preserved reflex evidence in monkeys (Bender and Shanzer, 1964). response (Hawkes, 1974). On double simultaneous Skew deviation was observed in our patient. The caloric stimulation, the observed vertical conjugate hypertropic eye was ipsilateral to the completely deviation of the eyes results from thermally- destroyed MLF. A review of the subject docu- induced currents in the endolymph of either the ments the observation that the elevated eye is unopposed anterior (resulting in reflex upgaze) or ipsilateral to the lesion in unilateral internuclear posterior (resulting in reflex downgaze) semi- ophthalmoplegia (Keane, 1975). It is possible that circular canals after antagonistic reflex gaze signals on the side of the lesion results from from the horizontal semicircular canals neutralise loss of a tonic downward component originating each other (Szentagothai, 1950; McMasters et al., in the vestibular nuclei and carried by a disrupted 1966; Pasik et al., 1969a). It has been shown MLF. The release of a tonic upward component, experimentally in monkeys that ascending fibres possibly of vestibular origin and conveyed by the from the vestibular nuclei project to the extra- contralateral MLF, may also explain the origin of ocular motor nuclei primarily via the medial the upward deviation of the eye in unilateral or longitudinal fasciculi, and that most axons in the incomplete bilateral MLF syndromes. It would MLF rostral to the abducens nuclei arise from follow that the relatively infrequent occurrence of both vestibular nuclear complexes (Carpenter skew deviation with complete bilateral MLF et al., 1963; Carpenter and McMasters, 1963; lesions results from a balanced loss of upward and Carpenter and Strominger, 1965; McMasters et al., downward tonic influences. 1966). Vertical vestibulo-ocular responses have Other lesions abolishing reflex vertical gaze been abolished by sectioning the MLF in primates would include labyrinthine, eighth , and http://jnnp.bmj.com/ (Evinger et al., 1977). Thus the clinical and experi- vestibular nuclear involvement bilaterally. Recent mental evidence support the concept that the reports suggest that pretectal lesions may also im- medial longitudinal fasciculi carry the innervation pair reflex vertical gaze in the absence of complete for reflex vertical gaze from the vestibular nuclei third and fourth nerve nuclear destruction to the oculomotor and trochlear nuclei. (Halmagyi et al., 1978; Reagan and Trautmann, Our patient demonstrated voluntary vertical 1978). In these syndromes, however, voluntary gaze, although the range of movement of upgaze vertical gaze is also significantly impaired. was limited. This observation has been made in We have reported a case of bilateral MLF in- other patients with diffuse cortical dysfunction volvement and impaired reflex vertical gaze with on September 24, 2021 (Critchley, 1956; Hurwitz, 1968; Adams and preserved voluntary vertical gaze. In addition, we Hurwitz, 1974; Jenkyn et al., 1977). Additionally, have noted a case in the literature of intact reflex it has been suggested that the neuronal pathways downgaze with the medial longitudinal fasciculi for vertical gaze are not direct, but proceed from as the only preserved ascending extraocular motor the pretectum to the rostral paramedian pontine pathways. We conclude that the major pathways J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

Reflex vertical gaze and the medial longitudinal fasciculus 1089 for reflex vertical gaze in man are the medial the medial longitudinal fasciculi in mediating reflex longitudinal fasciculi. These observations do not vertical gaze. imply a centre for reflex vertical gaze. Rather, they stress the importance of separate pathways We wish to thank Judy Murphy for her efforts in (Fig. 4) for voluntary and reflex vertical conjugate preparation of the manuscript, and Val Page for eye movements and the probable role played by the medical illustrations.

DORSAL VIEW DORSAL VIEW

N -_ PC MIDBRAIN MIDBRAIN

PONS PON S by guest. Protected copyright.

MEDULLA \IHWXAS \-- |CORTICA PATHWAYS \ I--- IErLEX \ 1..... POS3WLE WECUSWIW. MEDULLA \I OOTICAL MHS ) --- REFLEX \ Innervation of voluntary and reflex horizontal gaze (.I I I POSSIBLE DECUSSATING | .. REFLEX PATHWAYSI (a) Innervation of voluntary and reflex vertical gaze (c) LATERAL VIEW MIDBRAIN PONS MEDULLA LATERAL VIEW MIDBRAIN PONS MEDULLA

PATHWAYS http://jnnp.bmj.com/ PATHWAYS ___ REFLEX CORTICAL --- REFLEX (...... POSSIBLE DECUSSATING CORTICAL PATHWAYS) Innervation of voluntary and reflex horizontal gaze Innervation of voluntary and reflex vertical gaze (b) (d) Fig. 4 (a and b) Dorsal and lateral schematic representations of the presumed pathways of voluntary and gaze. The exact decussation axons into the contralateral

reflex horizontal level of of the corticobulbar on September 24, 2021 PPRF is not known and may take place at multiple levels. (c and d) Dorsal and lateral schematic representations of the presumed pathways of reflex vertical gaze. Innervation of voluntary vertical gaze requires an intact pretectal region, posterior commissure, and rostral pontine paramedian reticular formation (stippled area). The exact neuronal pathways within this area are not known. PC=posterior commissure; SC=; IC=; III N=; IV N=; VI N=; MLF-medial longitudinal fasciculus; PPRF=paramedian pontine reticular formation; VEST N=vestibular nucleus; RN=. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.41.12.1084 on 1 December 1978. Downloaded from

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