Journal of Neuro-Ophthalmology, March 1990, Volume 10, Issue 1

Oculographic analysis of acute esotropia secondary to a thalamic hemorrhage.

We used electrooculography to study the saccadic velocities, smooth pursuit, and vestibular ocular reflex in a patient with an acute thalamic hemorrhage. Our findings confirmed what others have shown in that there were hypometric saccades contralateral to the lesion, impaired smooth pursuit ipsilaterally, and a preserved vestibular ocular reflex. In addition, we demonstrated an asymmetry with the contralateral eye being more affected. It is also shown that the "convergence" movements seen on attempted upgaze are typical of saccades and not vergence movements. A discussion of possible pathophysiologic mechanisms with review of other studies is presented.

Journal of Clinical Neuro- ophthalmology 10( 1): 21- 26, 1990. Oculographic Analysis of Acute Esotropia Secondary to a Thalamic Hemorrhage Richard W. HertIe, M. D., and Don C. Bienfang, M. D. © 1990 Raven Press, Ltd., New York We used electrooculography to study the saccadic veloc­ities, smooth pursuit, and vestibular ocular reflex in a patient with an acute thalamic hemorrhage. Our find­ings confirmed what others have shown in that there were hypometric saccades contralateral to the lesion, im­paired smooth pursuit ipsilaterally, and a preserved ves­tibular ocular reflex. In addition, we demonstrated an asymmetry with the contralateral eye being more af­fected. It is also shown that the " convergence" move­ments seen on attempted upgaze are typical of saccades and not vergence movements. A discussion of possible pathophysiologic mechanisms with review of other studies is presented. Key Words: Thalamic hemorrhage- Saccades­Esotropia. From the Department of Ophthalmology,. The University Hospital and Boston City Hospital, Boston UniversIty School of Medicine, ( R. W. H.) and Department of Ophthalmology, The Brigham and Women's Hospital, Harvard Medical School, Bos­ton, Massachusetts, U. S. A. 21 According to Walsh et al. ( 1), thalamic hemor­rhage accounts for 2'>- 35% of all cerebral hemor­rhages diagnosed by computerized tomography. Fisher ( 2) localized 13% of intracerebral hemor­rhages to the thalamus. Castaigne et al. ( 3) divided them into three categories based on topographical and vascular arrangements: unilateral parame­dian, bilateral paramedian thalamic, and parame­dian thalamopeduncular. They concluded that paramedian thalamic infarcts were rarely isolated. The mesencephalic gray matter, principal nucleus, and fibers of the third cranial nerve were affected in > 75% of cases. Symptoms from thalamic hemorrhage include altered levels of consciousness from hypersomnia to deep coma, behavioral disturbances, impaired memory, abnormal clonic or atheototic move­ments, speech and language dysfunction, and oc­ulomotor disturbances ( 1- 3). Fisher ( 2) described the oculomotor signs as con­vergence spasm, paresis of horizontal and vertical gaze, downward deviation, and miotic, poorly re­active pupilS. Other signs may include ptosis on the involved side and a skew deviation during the acute stage ( 3,4). Full vestibularly driven eye movements, decreased convergence and Bell's phenomenon, and " nystagmoid jerks" are also re­ported ( 2). Brigell et al. ( 4) reported a case with transient opsoclonus, hypometric saccades contra­lateral to the lesion, and low gain pursuit ipsilat­erally. Wall et al. ( 5) described three cases of rostral midbrain and thalamic infarction with paresis of vertical gaze, absent convergence, aneisicoria, variable response to vestibularly driven eye move­ments vertically, and decreased pupillary re­sponses to both light and near. Ochs et al. ( 6) found opposed adducting saccades on attempted upgaze in their eye movement recordings of a pa­tient with a thalamic tumor extending to the mid­brain causing Paurinaud's syndrome. 22 R. W. HERTLE AND D. C. BIENFANG The associated findings of impaired vertical gaze, convergence spasm ( acute esotropia), con­vergence retraction nystagmus with attempted up­gaze, and miotic poorly reactive pupils constitute Parinaud's syndrome described in 1883 and later elaborated on by Koerber in 1903 ( 7). Investiga­tions into the pathophysiology of the oculomotor disturbances by Gay et al. ( 8), using electromyog­raphy, showed cocontraction of all muscles tested during retraction. There was an abrupt onset of electromyographic activity consistent with a sac­cadic discharge ( 8). Esslen and Papst in 1961 found excessive tonic electromyographic activity resem­bling spastic innervation from disinhibition of the superior and inferior recti motor nuclei as well as faulty recruitment of motor units in the superior rectus. Daroff and Hoyt ( 8) found no evidence of horizontal vergence movements during retraction, but a pattern of horizontal dysjunctive saccades of unequal amplitude towards the center. We recently had the opportunity to perform oc­ulography on a patient with an acute thalamic hemorrhage. The results with subsequent discus­sion are reported below. CASE REPORT An 84- year- old right- handed white woman had a history of coronary artery disease and hyperten­sion. She noticed the acute onset of perioral numb­ness that spread to both sides of her body. At the same time, she noticed severe right- sided head­ache, diplopia, dizzyness, nausea, and left- sided weakness. She fell while attempting to rise out of a chair and hit her left temple. She had slurred speech while calling her daughter on the phone and was brought to the emergency room. Past medical history was significant for a myo­cardial infarction 6 years previously and cataracts. Physical examination in the emergency room re­vealed an 84- year- old white woman in no acute distress. Her blood pressure was 180/ 85, pulse 72 with premature ventricular contractions ( PVCs), and respirations 14- 18/ minute regular and un­labored. There was a fresh 3.0- cm contusion over her left temple. Neurological exam showed orien­tation to person and place, decreased attention, normal memory, and dysarthria, and cranial nerve examination showed mildly decreased sensation of the left face and central facial weakness. She had a dense flacid left hemiparesis, decreased sensation on the left, and upgoing toes bilaterally. Her ocu­lomotor examination at the time of admission was reported to show miotic poorly reactive pupils to direct light. convergence spasm, limitation of up- I LIm Neu{ v- uIJftliwlliiul, ', 101' , t" i 1 I~) CIIJ gaze with convergence on attempt, and increasing convergence on downgaze. The patient's medical status prohibited examina­tion in the ophthalmology office at anytime during the hospitalization, and some tests, such as calo­rics, were felt to be too strenuous for her. Oph­thalmologic consultation in the intensive care unit 1 day after admission revealed 2.5- mm pupils poorly reactive to both direct and consensual stim­ulation. There was a 30- 40 prism diopter esotro­pia, which increased on downgaze simulating a V- pattern. This was measured with the patient fix­ating a target at 15 ft while performing both the cover- uncover test and the simultaneous prism­cover test. There seemed to be a preference for the right eye, but she freely alternated fixation. There was limitation of up gaze to - 10° with " convergence" movements on attempt. The pa­tient responded to commands with limitation of abduction bilaterally. The right abducted to 60% of normal and the left to only 10% of normal. There appeared to be sluggish convergence. Vestibu­larly driven eye movements showed full horizontal versions. Optokinetic movements using an opto­kinetic drum showed occasional convergent move­ments with downgoing stripes. There was also an intermittent, small amplitude, high frequency, ro­tary nystagmus that increased in intensity on up­gaze. The remainder of her ocular examination was normal except for bilateral cataracts and reti­nal vascular disease consistent with arteriolarscle­rosis and hypertension ( Fig. lA- F). Over the course of her hospital stay, all her physical findings improved slowly and steadily. Computerized tomography ( CT) at the time of admission showed a right midbrain hemorrhage extending rostral to the thalamus and into the mid­brain. There was no midline shift of intraventricu­lar or subarachnoid hemorrhage ( Fig. 2A and B). RECORDING METHOD A Traucoustics model # BV- 275 saccadic velocity recorder that has DC coupling and a bandwidth of 0- 75 Hz was used. This unit is portable enough to be used at the bedside, which is where the record­ings were done. Electrodes were placed both tem­porally and nasally as well as a ground on the fore­head. The stimulus apparatus was a Traucoustics model # RV- 259 Digital Light Bar. This contains light- emitting diodes placed so as to subtend visual angles of 5°, 10°, and 15° both horizontally and vertically 1.5 m from the patient. The patient's head was held steady as she was asked to look at the test lights. The protocol involved both binocu- ESOTROPIA AND THALAMIC HEMORRHAGE 23 ,..' D E FIG. 1. Oculomotor exam performed one day after the patient's cerebro­vascular accident. Photographs were taken at the patient's bedside. A: Pa­tient with gaze straight ahead showing both eyes turned in. Acute esotropia. B: Patient asked to look right with limitation of gaze more evident in ab­ducting right eye. C: Patient asked to look left with limitation of gaze more evident in the abducting left eye. 0: Patient asked to look up with obvious limitation of vertical gaze. E: Patient asked to look down showing some limitation but less than in upgaze and increasing esotropia. F: Vestibularly driven eye movements to the left showing full versions in abduction. G: Vestibularly driven eye movements to the right showing full versions in abduction. lar and monocular saccades between center and 10°, and center and 15° lights. Upward saccades to a 10° light was attempted as well. Smooth pursuit was evaluated grossly with the patient instructed to follow a hand held target moving at - 5- lOo/ s in a sinusoidal pattern. The vestibular reflex was tested by asking the patient to view the central diode while the head was manually rotated. RESULTS Electrooculography was performed on the 10th day after the patient's cerebrovascular accident. With the right eye, viewing attempts were made between 15° right and 15° left. The first and third abductive saccades had a gain of close to 1. The first and second adductive saccades were hypo­metric with no corrective saccade made after the first adductive saccade and a small glissadic- like movement followed by a corrective saccade made after the second. Five millimeters equals 2.5° for calibration on the position trace. Average velocities were 244°/ s in abduction and 229°/ s in adduction calculated for all 15° saccades made during this paradigm ( Fig. 3A). With the left eye viewing center to 15° right ( the patient was unable to voluntarily abduct very far past the midline), there was hypometria in both directions but more severe in abduction compared to adduction. The three adductive saccades have a gain close to 1 and are followed by small additional saccades. The three abductive saccades clearly re-quire more saccades to arrive at the target. The calibration of this position trace is 1.0 mm equals 1.0°. Averages of adducting saccadic velocities were 193°/ s and abducting velocities were 71°/ s cal­culated for all voluntary or involuntary saccades of 5° made during this paradigm. With both eyes viewing and attempted upgaze to 10°, bilateral convergence was seen. This con­sisted of an adducting saccade in both the right and left eyes. The average velocities of these sac­cades were 45°/ s in the left and 42°/ s in the right as calculated for all saccades measuring 5° during this paradigm ( Fig. 3C). Because of lack of sensitivity inherent in elec­troOCUlography ( EOG), the involuntary oscillations are not fully appreciated in the recording, but there can be seen brief periods of the horizontal component of the oscillation on attempted upgaze. They appear pendular with a jerk component. The position calibration is 1.0 mm equals 1.0° ( Fig. 3D). Smooth pursuit showed low gain in both direc­tions. With the right eye viewing, the gain to the right was 0 as evidenced by total saccadic replace­ment. Gain to the left, although close to 0, did show evidence of some intact pursuit ( Fig. 3E). The vestibular ocular reflex was relatively well pre­served with the right eye fixating ( Fig. 3F). DISCUSSION The most obvious disturbance in this patient is the esotropia. In hysterical individuals, conver- I Clin Neuro- ophthalmol. Vol. 10. No. 1, 1990 24 R. W. HERTLE AND D. C. BIENFANG FIG. 2. CT scan ot tne neao on aa'mlssion. A: Hemor­rhage in the right posterior thalamus. B: Higher mag­nification in the coronal plane showing hemorrhage in the posterior medial thalamus and midbrain. gence is usually associated with accommodation ( 7). Convergence has been described in patients with basilar inflammation following head trauma and as a consequence of hyperopia with a high ACiA ratio ( 7). Mott and Schafer, in 1960, pro­duced convergence in eyes of monkeys by bilateral stimulation of corresponding areas of frontal lobes or occipital eye fields. lampel, in 1959, elicited asymmetric convergence movements associated with variable miosis and accommodation with uni­lateral stimulation of points in the primate's occip­ital cortex. In primates, Pasik et al. ( 9,10) obtained adduction of the ipsilateral eye from an area of the tegmentum lying ventrolaterally at the rostral end of the midbrain. Both convergence and downward deviation of the eyes were obtained by stimulation ( If th,' n'" to'fl' , r ' c,'~ rr';'> ry thalamus 13 mm lateral to the midline. In humans, Moster and Hoenig ( 11) reported a case of intermittent " convergence spasm" secondary to metabolic encephalopathy, and Selhorst ( 12) reported two patients with acute esotropia secondary to thalamic hemorrhage. From the preceding animal work and human ob­servation, several areas of cortical and subcortical stimulation could produce convergence. Patients with acquired convergence have lesions that are destructive and not thought to be a cause of exces­sive stimulation. Selhorst ( 12) postulated, in his two patients, loss of supranuclear inhibition of convergence to be responsible for the acute esotro­pia. In studying the convergence system in hu­mans, Schor and Cuiffreda ( 13) postulates a con­stant tonic vergence system that operates indepen­dently of both accommodative and proximal vergence. It functions to align the eyes from an anatomical position of rest with a possible role in active convergence ( 13). In our patient, the neural integration between the different types of ver­gence may be disrupted resulting in an excess of convergence. The associated miosis makes a large contribution from the accommodative component seem highly likely. We know that there is constant neuromuscular activity in the extraocular muscles that is their " tone" and that the only time no recordable activ­ity is found in an inhibited antagonist muscle palsy manifest as an imbalance of tone or spasticity ( 14). Because our patient's esotropia could be over­come by vestibularly driven eye movements, it may be a form of pseudo CN VI palsy ( 15). Impaired vertical gaze is seen in a variety of su­pranuclear, nuclear, and infranuclear disorders. This seems always to be the result of a bilateral lesion, either directly or involving a decussation. The important areas are the posterior commissure, the rostral interstitial nucleus of the mediallongi­tudinal fasiculas, the rostral medial longitudinal fa­siculas, and the interstitial nucleus of Cajal ( 9,10,16,17). In patients with thalamic hemorrhage, Brigell et al. ( 4), Hirose et al. ( 18), and Masdeau et al. ( 15) reported hypometric saccades contralateral to the side of the lesion. They postulate that interruption of direct synaptic connections from the prefrontal cortex through the thalamus, specifically the " transthalamic bundle," simulate a decorticate state for saccadic activity. Monkey studies have shown similar abnormalities after decortication ( 19). It is interesting that we found the contralateral eye to be more affected. This was true in Selhorst's ( 12) two cases of acute esotropia secondary to thalamic hemorrhage. One could postulate both contralat- ESOTROPIA AND THALAMIC HEMORRHAGE 25 ... ,. ..... Tl - Ol' =.£.' .1. - c . , --- - .... · ..., L,... ;~ IJiio.~~" 1.""~~ rQ : s ~ F FIG. 3. Oculomotor recordings completed 10 days after the patient's cerebrovascular accident. Velocities were either 40 0 / s/ cm or 200 0 / s/ cm as marked on each recording sample. Calibration for position was 5.0 mm equals 2.5° or 3.0° as marked on the photograph and described in the text. Rightward eye movements are up and leftward are down on each of the position traces. A: Right eye ( 00) viewing with saccades attempted between 15° right and 15° left showing hypometria in both abduction and adduction but greater in adduction ( contralateral to the lesion). See text. B: Left eye ( OS) viewing center to 15° right ( patient could not voluntarily abduct much beyond midline) again with hypometria in both directions with a more profound difference between abduction and adduction. It is worse in abduction, contralateral to the lesion. C: Saccades made between center and 10° up with representative velocity tracings from both eyes. Oysjunctive movements with saccadic characteristics are evident. These are convergent and correlate with the clinical appearance of convergence on attempted upgaze ( arrows). D: Position traces of same saccades between 10° up and center showing bilateral adduction saccades and oscillations. See text for details. E: Right eye smooth pursuit was tested to a hand- held target moving in a sinusoidal pattern at - 5- 100 / s with the head held stationary. This shows symmetrical low gain pursuit at almost 0 gain but occasional pursuit was seen to the left ( contralateral to the lesion). F: Vestibular ocular reflex with the 00 fixating a central target. This shows a well- preserved reflex with almost a gain of 1.0. eral cortical control, not only of saccadic gaze, but also uniocular saccades of the contralateral eye. Our patient also had impaired smooth pursuit. It was not as easy to see the asymmetry in our pa­tient as it was in the patients reported by Hirose et al. ( 18) and Brigell et al. ( 4). Pursuit was more im­paired ipsilateral to the lesion. Although not as well understood as the saccadic system, interrup­tion of descending fibers from the inferior parietal lobe or peristriate cortex in and around the thala­mus could interfere with smooth pursuit. Leigh and Zee ( 14) say that low gain pursuit can be at­tributed to large lesions of the human parietal lobe and the impairment is ipsilateral. The convergence retraction seen in our patient and those with Parinaud's syndrome is not a true convergence movement but either a cocontraction of all extraocular muscles or impaired saccadic dy­namics ( 6- 8). Hypotheses to explain these movements include a " diffuse spread" of voluntary impulses, in which the medial rectus, being the largest, caused con-vergence; isolated medial recti activity; and an ex­aggerated stretch reflex ( 6- 8). Ochs et al. ( 6) have shown the fine structure of these eye movements and proposed a more phys­iologic explanation. These opposed adducting sac­cades are the result of a normal dynamic overshoot mechanism operating at high gain in the contralat­eral eye. This explains their observed asynchro­nous initiation and the convergent movement. The normal lower level brain stem is modified by high­gain signals. In summary, an upward eye move­ment attempt is followed by a contralateral di­rected conjugated saccadic impulse that is modi­fied by a supranuclear high- gain instability to the contralateral eye, causing a large dynamic over­shoot manifesting clinically as opposed adducting saccades or " convergence" ( 6). The variety of oculomotor abnormalities seen with thalamic hemorrhage imply involvement of tracts going through the thalamus, near the thala­mus, or coincidental involvement of nearby struc­tures. As Castaigne et al. ( 3) found in their study of JClin Neuro · ophthalmol. Vol. 10, No. 1, 1990 26 R. W. HERTLE AND D. C. BIENFANG 28 patients, at least 50% had oculomotor abnormal­ities. Paramedian thalamic or midbrain infarcts are rarely isolated, and they often involved the mes­encephalic grey and third cranial nerve. These pat­terns are inconstant and dependent on variation in blood supply and etiology of destruction. Oculo­motor findings consisted of parts of or the com­plete Parinaud's syndrome plus variable third nerve involvement. Attention to these deficits can be clues to the diagnosis of thalamic hemorrhage. REFERENCES 1. Walsh TM, Davis KR, Fisher CM. Thalamic hemorrhage: a computed tomographic correlation. Neurology 1977; 27: 217­22. 2. Fisher CM. The pathologic and clinical aspects of thalamic hemorrhage. Trans Am Neural Assoc 1959; 84: 56. 3. Castaigne P, Lherrnette F, Buge A, Escourolle R, Hauw H, Luon- Caen O. Paramedian thalamic and midbrain infarcts: clinical and neuropathological study. Ann Neural 1981; 10: 127- 48. 4. Brigell M, Babikian V, Goodwin JA. Hypometric saccades and low gain pursuit resulting from a thalamic hemor­rhage. Ann Neural 1984; 15: 374- 8. 5. Wall M, Slamovitz TL, Weisberg LA, Trafant SA. Vertical gaze ophthalmoplegia from infarction in the area of the posterior thalamo- subthalamic paramedian artery. Stroke 1986; 17: 546- 53. 6. Ochs AL, Stark L, Hoyt WF, D'Amico P. Opposed adduct­ing saccades in convergence retraction nystagmus: a pa­tient with sylvian aqueduct syndrome. Brain 1979; 102: 497­508. 7. Daroff RB, Hoyt WF. Supranuclear disorders of oculomotor control systems in man: clinical, anatomical and physio- J Clm Nt1uru · ophJhulnwJ. \ lvl. JI;, : Ju. i. l~/' iU logic correlations. In: Bach- y- Rita, Collins, Hyde, eds. The control of eye movements. New York: Academic Press, 1971: 175- 235. 8. Gay A, Brodkey J, Miller J. Convergence retraction nystag­mus: an electromyographic study. Arch OphthalmoI1963; 70: 62- 7. 9. Pasik P, Pasik T, Bender MB. The pre- tectal syndrome in monkeys. I. Disturbances of gaze and body posture. Brain 1969; 92: 521- 34. 10. Pasik P, Pasik T, Bender MB. The pre- tecta! syndrome in monkeys. II. Spontaneous and induced nystagmus and " lightening" eye movements. Brain 1% 9; 92: 871- 4. 11. Moster ML, Hoenig EM. Organic convergence spasm with metabolic encephalopathy [ Abstract]. Presented at the 12th Annual Rocky Mountain Neuro- ophthalmological Society, 1986. 12. Selhorst JB. Acute esotropia. Presented at The Frank B. Walsh Society, 19th Annual Meeting. 13. Schor C, Cuiffreda KJ. Vergence eye movements: basic and clin­ical aspects. Butterworths, 1983: 1- 92. 14. Leigh RJ, Zee D. The neurology of eye movements. F. A. Davis Co., 1983: 6~ 8. 15. Masdeu T, Brannegan G, Rosenburg A, Dobrin S, Hires R. Pseudoabducens palsy with midbrain lesions. Ann Neural 1980; 8: 103. 16. Meissner 1, Sapir S, Kolomen E, Stein SD. The paramedian diencephalic syndrome: a dynamic phenomenon. Stroke 1987; 18: 380-- 5. 17. Pierrot- Deseilligny CH, Grey F, Serdaru M, EscouroUe F, Lhermitte F. Parinaud's syndrome: electrooculographic and anatomical analysis of six vascular cases with deduc­tions about vertical gaze organization in the pre- motor structures. Brain 1982; 105: 667- 96. 18. Hirose G, Kosoeqawa H, Saski M, et al. The syndrome of posterior thalamic hemorrhage. Neurology 1985; 35: 998­1002. 19. Sharpe J, Rabinovich J. Control of the saccadic and smooth pursuit systems after cerebral heidecortication. Brain 1979; 102: 387- 403. 20. Zee D, Robinson D. A hypothetical explanation of saccadic oscillations. Ann Neural 1979; 5: 405.