J. Neurol. Neurosurg. Psychiat., 1957, 20, 139.

DISORDERS OF OCULOMOTOR FUNCTION IN LESIONS

OF THE OCCIPITAL LOBE*BY

MORRIS B. BENDER, DONALD M. POSTEL, and HOWARD P. KRIEGER

From the Departments of Neurology ofNew York University, Bellevue Medical Centre, and the Mount Sinai Hospital,New York City

The physician and even the neurologist associatesthe occipital lobe with visual functions. Rarelydoes one attribute motor disturbance to lesions inthis region of the brain. While there is no doubtthat normal vision is dependent on intactness ofthe calcarine cortex and the subcortical opticradiations, there is apparently little clinical evidenceto indicate that the occipital area plays a role inthe movements of the eyes. From experiments inanimals and cortical stimulations in man it isapparent that the occipital lobe must have aninfluence on eye movements.

In monkeys various types of eye movements havebeen elicited from the occipital cortex and sub-cortex (Shafer, 1888; Luciani and Tamburini, 1879;Grunbaum and Sherrington, 1901; Walker andWeaver, 1940; Crosby and Henderson, 1948; Lilly,Hughes, and Galkin, 1956; Krieger, Wagman, andBender, 1955). While these effects are easilyobtained in the alert and less readily in theanaesthetized monkey, ocular deviations are difficultto elicit on electric stimulation of the occipitalcortex in man. Walker and Weaver (1940) statedthat eye movements can be elicited from theoccipital area in all animals but man. Foerster(1931), on the other hand, stated that ocular devia-tions could be evoked on stimulation of area 19but not areas 18 or 17. Penfield and Boldrey (1937)reported two cases with contralateral ocular devia-tion after stimulation of area 19. However, in 1950Penfield and Rasmussen stated that in 31 patients48 loci for eyeball movement were found and " allwere located rostral to the central sulcus ". Toexplain the previous observations the followingfootnote is then added: " In earlier operations inwhich less physiological stimulating currents wereused, eye turning was elicited in one patient fromthe temporal lobe and in three patients from the

parietal lobe ". The latter three patients includethe two in whom eye movements were elicited fromarea 19. Penfield similarly accounted for thedifference between his and Foerster's results bynoting that the latter used much stronger stimuliand evoked adversive convulsions including theeyes. In their work Penfield and his associates(Penfield and Boldrey, 1937; Penfield and Rasmussen,1950) did not consider any epileptiform reactionsas positive results. However, in recent work onthe monkey with implanted electrodes Lilly andhis colleagues (1956) have evoked adversion, in-cluding the eyes, upon stimulation of the lateralsurface of the occipital lobe and not isolated eyemovements.

While there are examples of excitatory influenceson eye movements produced by stimulating theoccipital lobe, there is very little information onoculomotor deficits as a result of lesions in this area.Gordon Holmes (1921) described defects in visualfixation and fusion movements of the eyes in gun-shot wounds of the occipital lobes. The so-calledvoluntary movements which remain are not perfect.For example, fixation other than straight forwardcannot easily be maintained and may be accompaniedby nystagmus. These abnormalities are found eventhough there is no paralysis of the individual eyemuscles involved. Thus it is reflex maintenance ofconjugate gaze in any one direction or even centeringof eyes which is defective and the chief complaintis usually blurred vision, which increases with anymovement of the line of vision. This blurred visionpersists with one eye closed, thereby differentiatingit from diplopia. Although bilateral occipital lobedamage is usually necessary for this syndrome,reflex maintenance of gaze may be defective uni-laterally. When it is bilateral it becomes even moremarked. The post-mortem examinations of cases byGordon Holmes (1921) revealed that this defectin fixation was related to "interruption of thecortico-tectal fibres which form the efferent link

139

* This work was aided in part by grants No. B-174 (S.D.) and No.B-294(C) from the United States Public Health Service.

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140 MORRIS B. BENDER, DONALD M. POSTEL, AND HOWARD P. KRIEGER

of the reflex arch; the disease involved the dorsalportion of the thalamus including the pulvinar".In addition, Gordon Holmes described occipitallesions as producing paresis of gaze to the sideopposite the lesion. In his cases this occurred onlyin hemianopics who were mentally obtunded,suggesting that what Holmes may have observed iswhat has been described as hemispatial inattentionor hemispatial agnosia. Dejerine and Roussy (1905)observed such paresis after a recent occipital injuryin a previously blind person, suggesting that visionis not the factor in these cases. Gordon Holmes(1921) also noted that many hemianopics could notaccurately fixate targets on the hemianopic side,despite preservation of macular vision and accuratefixation of a target in the midline. Holmes concludedthat such a defect could not be due to visual lossbut was due to unilateral loss of the visual reflexesneeded for maintaining the position of the eyesachieved by voluntary ocular movement.

In contrast to these observations and deductionsare those of Penfield and Rasmussen (1950). Theyamputated one occipital lobe and found the onlydefect to be a contralateral homonymous hemianopia.There was no difficulty in oculomotor functions.Excision of the occipital cortex outside the calcarineregion produced no defect in vision or oculomotorfunction of which the patient was aware. Destruc-tion of the occipital lobe in monkeys leads tocontralateral hemianopia and at most to a transientdefect in contralateral conjugate gaze which isassociated with turning of the entire body about itslong axis in the direction of the side of thelesion.The present study concerns alterations in oculo-

motor activity appearing subsequent to lesions ofthe occipital lobes in two patients.

L.E. R.E.

Case 1.-D. G. developed hypertension (160-1701100-110 mm. Hg) at the age of 33. At 37 years of agehe suffered, in rapid succession, a coronary occlusion,a popliteal thrombus, multiple pulmonary infarcts, andan embolus to the right posterior cerebral artery. Thelatter was followed by an almost congruent left homony-mous hemianopia, spots before the eyes, and blurredvision. In 1949, at the age of 41, he was completelyblind for one hour. This was followed by left-sidedblindness and the subjective experience of being draggedto the left by the head and eyes.The patient was admitted to the Mount Sinai Hospital

for special studies. The visual sensory symptoms andsigns of this patient just after the episode of completeblindness have been reported previously (Bender andKahn, 1949). Essentially, there was an incongruent lefthomonymous hemianopia with scotomas and a smallrelative scotoma in the right upper quadrants (Fig. 1).These defective fields were the site of trouble in per-ception of motion, form, distance, colour and after-imagery. Additional signs of neurological disease werehyperaesthesia of the left upper lip and right wrist. Therewas transient evidence of a hemiparesis affecting theright foot. Radiographs of the skull, the cerebrospinalfluid, and an electroencephalogram were normal. Thediagnosis was bilateral and successive occlusion of theposterior cerebral arteries.The most marked oculomotor defect found after the

second occlusion was nystagmus on fixation of a targetduring deviation of the eyes to the side of the maximumfield defect (left). The nystagmus was a shimmering,cogwheel type of eye movement apparent on attemptedfixation of a target at the near point. During fixationat a distance this nystagmus was absent. When present,at a near point, nystagmus was most marked in thefixating right eye, the non-fixating eye being turnedinward, giving it the appearance of making a strongattempt at convergence. Nausea and vertigo developedwhen such fixation was prolonged.Double vision was experienced during fixation at the

near point or at a distance. If the patient looked at his

FIG. I.-Perimetric and tangent(opposite page) screen visualfields of D. G. illumination,daylight; 5 mm. white targetat 33 cm. Solid black, absenceof perception of motion.Vertical lines, movement per-ceived but marked blurring

£067s'' ~~~and fluctuation in appearanceof target. Stippling, target lessblurred. Small circles andhorizontal dashes, blurred orgrey vision. The dashes in theperimetric fields outline thefield of vision for the colourred.

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own finger he saw two parallel fingers one overlying theother. He called this experience " transparency" sinceeach finger was seen in its entirety despite the overlap.The degree of image separation increased the fartherthe target was removed from the patient. This diplopiawas best demonstrated by turning the head to theextreme left while the eyes were turned to the right anddown, that is, toward the least defective field of vision.Under these conditions a target in the left or defectivefield was seen with an associated false image slightlyhigher as well as to the left of the real image. Markedbilateral nystagmus accompanied any attempt to fixateunder these conditions. Concomitantly, the non-fixatingeye converged.

Fifteen months after the onset of this oculomotordisturbance the patient was admitted to Bellevue Hospital.At this time a marked dissociated nystagmus was observedwhenever the patient attempted to fix an object in hisleft field of vision. Shortly afterwards he died in cardiacfailure.

Post-mortem examination was limited to the brainwhich showed infarction of the under surface of bothoccipital lobes (Figs. 2a and 2b). The infarct was largeston the right side extending forward but not into the

FIG. 2a.-Photograph of the inferior surface of the brain of D. G.The right occipital lobe is the site of an infarction throughoutits inferior aspect. Most of the posterior part of the right lingualgyrus is missing exposing branches of the posterior cerebralartery lying within the calcarine and other fissures. The inferiorsurface of the remnants of the right cuneus is exposed. Mostof the right occipital pole is destroyed. The inferior surface ofthe left occipital lobe is less severely damaged, the major destruc-tion occurring in the lingual and fusiform gyri rostrally and thusaffecting mainly the peristriate and parastriate areas.

FIG. 2b.-Representative coronal sections through each occipital lobe demonstrating the depth of the lesion. The right lobe is more extensivelyinvolved.

141

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142 MORRIS B. BENDER, DONALD M. POSTEL, AND HOWARD P. KRIEGER

temporal lobe and including Brodman's area 18, thatpart of area 17 lying below the calcarine fissure, and allof the tip of the occipital lobe. The lesion on the leftwas limited to a small region mainly of area 18. Therewere no lesions in the brain stem.

Case 2.-G. S. K., aged 57, first experienced a clonic,adversive seizure affecting the head and eyes at the age of26. This patient was first studied by Foerster in 1925and 1926. Since then these attacks have recurred weeklyand occasionally two or three times in one week. Duringthe first two years consciousness was lost three times.The attacks have consisted of a sensation of something

Fin(. 3.-Lateral and anterior-posterior views of the skull of G. S. K.

demonstrating the calcific lesion within the right occipital lobe.

impending, followed by anxiety, then a sensation ofblood or warmth rushing to the head, and finally clonicjerking of the head and eyes to the left superimposedupon tonic adversion of these parts to the same side.Each attack lasted a few seconds. The tongue was notaffected. Occasionally paraesthesias affecting the leftlower extremity and possibly the left hand appeared afteran attack. There was no diplopia, blurred vision, opticillusions, or. visual hallucinations. Four years beforethe first attack the patient was in a train accident. Hesuffered a blow to the head but did not lose consciousness.No other aetiological agent is known.The patient was examined at the office of M. B.

Bender on June 20, 1947, and again in 1953. The neuro-logical and mental states did not reveal any abnormality.An electroencephalogram was normal in 1947 andagain in 1956. Repeated radiological examinations of theskull have shown a right occipital calcified mass whichhas not grown in size (Fig. 3). It is assumed that theanatomical site of the lesion which causes the adversivehead and eye movements to the left is in the right occipitallobe and manifested by the calcification.

DiscussionIn summary, two cases of disturbances in oculo-

motor function associated with lesions of theoccipital lobe have been described. One hadunilateral disease, the other bilateral sequentialdisease. The common symptom was abnormalrepetitive eye movements. The case of unilateralcalcification in the occipital lobe had contraversiveattacks, the other had nystagmus when attemptingto fix in his most defective field of vision. It shouldbe stressed that this patient had a visual field defect.These two cases thus support the concept that

in man the occipital lobe participates in oculomotorfunctions. This is in agreement with Foerster's(1931) observations and those of workers who haveexperimented with animals. It may be asked whethersuch concepts as the visual fixation reflex and thetheory of balance between the forces effected througheach occipital lobe may help in analyzing these twocases.The nystagmus of the case with bilateral disease

was apparently the type associated with defects inthe postulated visual fixation reflex. It will berecalled that the nystagmus became most markedwhen the eyes were turned toward the most defectivevisual field while the head was turned in the oppositedirection. It is possible to agree with Holmes (1921)and say that this was nystagmus secondary to adefective fixation reflex since vision was partlyintact. However, it is not altogether clear why theposition of the head should play a role in thissymptom and why, as in the second case, it ispossible to have attacks of clonic adversive eyemovements without evidence of a fixation deficitor visual experience.

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DISEASES OF OCULOMOTOR FUNCTION

A definite answer cannot be given but somesuggestions arise from known experimental data.Shafer (1888) showed that the two cerebral hemis-pheres were in physiological balance as far aseffecting forces which move the eyes in the horizontalplane, each hemisphere exciting contralateral con-jugate deviation. Sherrington (1893) demonstratedthat there were active inhibitory forces also involvedin these horizontal conjugate movements. Bender(1955) postulated a third set of vectors, the centeringforces or those which bring the eyes to the mid-position and constantly counteract the deviationforces. If the existence of these forces is grantedthen it may be proposed that the altered oculomotoractivity observed in the two cases under considera-tion had a common physiological mechanism,namely, imbalance among the generators of theseforces, whether these generators lie in the anatomic-ally diseased structures or some other place alongthe pathways which pass through these structures.Such an explanation does not invoke centres forspecific types of horizontal or other eye movementsand it poses the problem in a form allowing anexperimental approach. Such a mechanism mightalso underlie the other oculomotor defects associatedwith the disease of the occipital lobes and commonlyexplained as loss of the " visual fixation reflex ".

There are observations tending to support sucha vector concept suggesting that all eye movements,normal and abnormal, are the result of forcesgenerated at many places along the neuraxis, i.e.,cerebrum, basal ganglia, brain-stem, cerebellum,vestibular nuclei, the various oculomotor nucleiand the retina, vestibular receptors and the pro-prioceptors of the head and neck (Bender, 1955;Spiegel and Sommer, 1944). Of particular interesthere are some recent observations on the monkey.It was noted that nystagmus could be induced in aconscious monkey if the animal's attention wereattracted ipsilaterally to an occipitally appliedelectric stimulus to the cortex. During such simul-taneous stimulation there was nystagmus (Kriegeret al., 1956). A possible interpretation of thisnystagmus is that it is the result of a rivalry betweenthe attention-engendered forces and the electrically-induced forces. Nystagmus was also noted uponstimulation of various parts of the occipital andfrontal eye fields without apparently requiring thefactor of attention. No particular anatomical orphysiological pattern was found for this nystagmus,suggesting that perhaps the effect of the addedstimulus was to create an imbalance between the

deviating and centering forces, which imbalance wasnoted as nystagmus.Why this imbalance appears as periodic, clonic

movements rather than tonic deviation cannot besaid. To state that the eyes partake in convulsivephenomena is descriptively true but adds little toour understanding of the mechanism whereby theabnormal activity of the occipital lobe tissue resultsin repetitive patterned contractions of the eyemuscles. Even if it were known how the calcifiedmass in Case 2 caused abnormal activity in theoccipital lobe, the question of why this was manifestas clonic eye movements while in a deviated positionstill remains open. There is no satisfactory physio-logical explanation for the two oculomotorsyndromes described in this paper. The occurrenceof these eye disturbances supports the concept ofoccipital lobe influence on oculomotor activity. Itis remarkable that so few cases of oculomotordeficit have been reported in disease of the occipitallobe. It would seem that this is an inadvertent errorof omission brought about by a combination of theprominence of the sensory defect and the usualclassification of the occipital lobe as a sensory organ.

SumnmaryTwo cases of defects in oculomotor activity are

described. One followed occlusion of both posteriorcerebral arteries; the other was associated with acalcified mass in one occipital lobe.The concept of the occipital oculomotor field is

reviewed and the pertinent conflicting data arepresented.

It is concluded that the occipital lobe influencesthe function of the oculomotor apparatus.

REFERENCESBender, M. B. (1955). A.M.A. Arch. Neurol. Psychiat., 73, 685.

and Kahn, R. L. (1949). Journal of Neurology, Neurosurgery,and Psychiatry, 12, 196.

Crosby, E. C. and Henderson, J. W. (1948). J. comp. Neurol., 88, 53.Dejerine, J., and Roussy, G. (1905). Rev. neurol. (Paris), 13, 161.Foerster, 0. (1931). Lancet, 2, 309.Grunbaum, A. S. F., and Sherrington, C. S. (1901). Proc. roy. Soc.,

69, 206.Holmes, G. (1921). Brit. J. Ophthal., 5, 241.Krieger, H. P., Wagman, I. H., and Bender, M. B. (1955). Trans.

Amer. neurol. Ass., p. 209.(1956) Ibid., pp. 112-114.

Lilly, J. C., Hughes, J. R., and Galkin, T. W. (1956). Fed. Proc., 15,119.

Luciani, L., and Tamburini, A. (1879). Rivista sperimentale difreniatria e di medicina legale, 5, 1-76.

Penfield, W., and Boldrey, E. (1937). Brain, 60, 389.and Rasmussen, T. B. (1950). The Cerebral Cortex of Man.Macmillan, New York.

Schafer, E. A. (1888). Brain, 11, 145.Sherrington, C. S. (1893). Proc. roy. Soc., 53, 407.Spiegel, E. A., and Sommer, I. (1944). Neurology of the Eye, Ear, Nose

and Throat. Grune & Stratton, New York.Walker, A. E., and Weaver, T. A. Jr. (1940). J. Neurophysiol., 3, 353.

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