Eccentric head positions reveal disorders of conjugate · JournalofNeurology, Neurosurgery, andPsychiatry, 1977, 40, 992-1002 Eccentric headpositions reveal disorders ofconjugate

Journal ofNeurology, Neurosurgery, and Psychiatry, 1977, 40, 992-1002

Eccentric head positions reveal disorders of conjugateeye movementM. GRESTY

From the Medical Research Council Hearing and Balance Unit, Institute of Neurology,National Hospital, Queen Square, London

SUMMARY The effect of head position on conjugate horizontal gaze was studied in healthyadults, in patients with multiple sclerosis without eye movement signs, and in patienits with down-beat nystagmus indicative of low brain stem lesions. Displacements of gaze from primaryposition to 300 left and right were recorded using the electro-oculogram, with the head in theprimary position, and turned voluntarily to the left and right (in yaw). The quality of eye move-ments was noted and peak velocities of saccades were measured. The head turning test trebledthe incidence of abnormal eye movements found in the multiple sclerosis patients and increasedit by tenfold in the patients with downbeat nystagmus. Disorders of eye movement were alsofound in approximately 20-30% of healthy subjects tested. Weakness of abduction was the mostcommon eye movement defect and appeared to be posterior internuclear ophthalmoplegia. Ahypothesis is made which unifies the theoretical explanations of anterior and posterior inter-nuclear ophthalmoplegia. The most likely cause of the disorders of eye movement observed isvertebrobasilar ischaemia induced by stretching and compression of the vertebral arteries duringeccentric head posture.

When the head is turned from its primary positionseveral things happen which have effects uponactivity within the central nervous system.

Firstly, if the head rotates in the horizontalplane (yaw) so that the chin points to the rightor left, the cervical spinal cord and the lowerbrain stem are deformed in torsion and shear, andthis may be accompanied by compression of oneside and stretching of the opposite side. Themechanical distortion of the brain stem probablyreaches as high as the level of the tentoriumcerebelli, and undoubtedly affects the cerebellarpeduncles and at least part of the body of thecerebellum (personal observations on the brainsof cats and monkeys fixed with the head held indifferent positions).

Secondly, displacement of the head in yawproduces differential movements between theforamen magnum, the atlas, and the axis whichlead to compression of the vertebral artery on theside towards which the head is turned and narrow-ing of the artery on the opposite side (De Kleyn andNieuwenhuyse, 1927; De Kleyn, 1939; Tissington

Accepted 26 May 1977

and Bammer, 1957). The mechanical effects of thespinal arteries may be also relevant. As a conse-quence of head turning local circulatory changesarise from neck muscle contraction and fromstretching, compression, and decompression effectson arteries, arterial baroreceptors, and veins. Nor-mally, compensations are made for the changesin circulation induced by head turning so thatadequate circulation is maintained. However, inthe presence of anatomical anomalies such asabnormally narrow arteries, or pathologicalchanges such as osteophytes which may deformblood vessels, head turning can produce insuffi-ciencies of cerebral blood flow.

Thirdly, head posture gives rise to a pattern ofproprioceptive signals from muscle and joint re-ceptors in the neck which have an important in-fluence on sensorimotor coordination (Longet,1845; Magnus, 1924; Cohen, 1961).The medulla, pons, and cerebellum contain

motor and important premotor centres for thecontrol of eye movements. Lesions in these centrescan give rise to disorders of eye movements whichcan be revealed by appropriate test procedures. Itmay be that the mechanical and vascular changes

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Eccentric head positions reveal disorders of conjugate eye movement

produced by head turning can heighten the degreeof oculomotor impairment and reveal latent de-fects not detectable with the head in its primaryposition. To investigate this hypothesis we havecompared displacements of horizontal gaze withthe head in its primary position with those exe-cuted when the head was turned to eccentricpositions, both in a group of normal subjects andin patients with a variety of diseases of the nervoussystem.

Saccadic velocities and conjugation of gaze wereselected for examination to minimise the involve-ment of postural reflex effects on eye movements.Vascular derangements and mechanical distortionremained as the main variables. Although postural(particularly neck) mechanisms are known toaffect eye movements in normal subjects (Meiry,1971) and in patients with nervous system diseases(Gray, 1956; Bos, 1962; Bos and Philipszoon,1963; Biemond and De Jong, 1969), it has not beendemonstrated that they influence either saccadicvelocities or the organisation of conjugate hori-zontal gaze.

Neurological testing with the head turned isnot new. The procedure has been used extensivelyin patients with cerebrovascular symptoms impli-cating abnormalities of the vertebral arteries(Biemond, 1951; Ford, 1952; Tissington andBammer, 1957; Sheehan et al., 1960). It has beenfound that head turning reveals a wide variety ofsymptoms indicative of vertebrobasilar ischaemia.However, we know of no reports of the test beingused comparatively in normal subjects and thetypes of patients we have surveyed, no attempts toquantify the results of head turning, and no studiesof its effects upon conjugate gaze.

Method

PATIENTS WITH NEUROLOGICAL DISEASESTwo groups of patients with central nervoussystem diseases were examined. One consisted offive patients between the ages 19 and 30 years whohad multiple sclerosis with no clinically observedocular signs. All were part of a longitudinal sur-vey conducted at the National Hospital and hadbeen observed for several years.The second group of patients was selected be-

cause they presented with the oculomotor sign of'downbeat nystagmus'. Downbeating nystagmus istaken to be a reliable sign of lesions of the lowerbrain stem and structural disorders in the regionof the foramen magnum (Cogan, 1968). Theseregions of the nervous system are the most likelyto be affected by mechanical or vascular con-comitants of head turning.

CONTROL GROUPSThe selection of normal subjects for controlgroups presented a problem because it required adefinition of normality. Several authors have des-cribed the eye movements of 'normal' subjectsduring displacements of horizontal gaze (Vossius,1960; Smith et al., 1970; Weber and Daroff, 1971;Bird and Leech, 1976), and all agree that thereare wide variations of accuracy, velocity, con-vergence, and conjugation of movement. Wecollected 15 subjects for controls and found thatin four of these the head turning test revealed eyemovements which appeared to be deranged. Theproblem was to decide whether the apparent de-rangements were simply unusual in that theyrepresented the extremes of statistical distributionof eye movement characteristics, or whether theeye movements were abnormal in the sense ofpathological. This decision was made with refer-ence to several criteria. The first and most import-ant criterion for an abnormal saccade was aconsistently low peak velocity. The secondcriterion was that the shape of the saccade wasconsistently degraded on repeated testing (com-pare, for example, the normal and abnormalsaccades in Figs. 2 and 3). In addition, whensaccades were made which appeared abnormal itwas sometimes found that other signs of oculo-motor impairment, such as nystagmus, were alsopresent. The velocity and shape of a particularsaccadic movement were compared with those ofthe same movement in different head positions,with those of the other subjects tested, and withthe data of other workers. If two or more of theabove criteria applied to a saccadic eye movement,the movement was judged to be abnormal and thesubject was excluded from the control groups.Examples of abnormal movements found in 'nor-mal' subjects are presented in group 2 of theresults.Two control groups with five subjects in each

were set up, divided into the age ranges of 19-31and 50-65 years respectively. The latter group canbe expected to include a higher incidence of vas-cular disorders. The subjects in the control groupsexhibited a wide range of saccade velocities; how-ever, the saccades they executed were consistentlywell formed and unaffected by head turning.

TESTING PROCEDUREThe subjects were required to execute saccadic eyemovements between a target in primary gaze andtargets 300 to the left and right, placed at a dis-tance of 700 mm with the head in the primaryposition and turned voluntarily to the left andright (illustrated in Fig. 1). Because of problems

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Fig. 1 Illustration of apparatus used to test saccadic eye movements. Subject makes eye movements tofixate targets on horizontal bar with head held voluntarily in three positions. The bar is supported by thesubject and stabilised with a chin rest.

of head mobility in some patients, predeterminedangular displacements of the head could not beachieved. Instead, subjects were asked to turntheir heads to the most eccentric positions theycould comfortably maintain. Displacementsgreater than 450 were achieved in all subjectstested, care being taken to ensure that when thehead was turned its sagittal plane remainedvertical.Eye movements were recorded using DC electro-

oculography, measurements of peak saccadicvelocities being made with a nomograph and re-stricted to saccades which were free from blinkand myogenic artefacts. As a result there werelimitations on the number of measurementsavailable.

Results

TESTING SIGNIFICANCE OF EYE MOVEMENT

ABNORMALITIES

In both patients and control subjects there werelarge interindividual differences in saccade velo-cities, and the data from each individual had highvariances. When disorders were revealed by headturning they followed idiosyncratic patterns whichcould not be easily tested against the normal con-trols. Accordingly, three criteria were chosen totest the significance of the findings.

1. The lower level of mean saccadic velocityfor healthy eye movements was set at 3200 second.This is a low value for any of our normal subjectsand gives a probability level of less than 2%. Itis also well below the criterion for normality setby Bird and Leech (1976) determined in the samelaboratory.

2. The patterns of changes of eye movement as

a function of head position were also taken intoaccount in each individual.

3. The statistics for a given eye movement andhead position were compared with those of thesame movement in the other positions in order todetect trends.

GROUP 1 SACCADIC MEASUREMENTS OF NORMALSUBJECTSNo degrading effects of head turning on conjugatehorizontal gaze were found in normal subjects.The findings are in agreement with other authors(Bird and Leech, 1976) who tested only in headprimary position, in so far as abduction was slowerthan adduction and decentring was slower thancentring. The younger group had slightly highermean velocities than the older controls who ex-hibited higher variances. The data are presentedin Table 1 for subjects in the age ranges 19-31and 50-65 years.

GROUP 2 ABNORMAL EYE MOVEMENTS REVEALED INNORMAL SUBJECTS BY HEAD TURNINGIn approximately 23% of the normal subjectstested, the head turning test revealed derange-ments of ocular motility. The derangements wereeither multiple, constituting a syndrome, or asingle defect was revealed. These observations willbe described in three subjects whose saccademetrics are detailed in Table 2.

Subject I-male, 56 years old. In all headpositions a right eye decentring and left eye cent-ring abduction weakness were present. With headturned to the right a first degree nystagmus waspresent in the right eye, and in the same eye ab-duction was badly formed and took a long time tosettle in the eccentric gaze position.

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Subject 2-female, 25 years old. With the headin primary position there was a weakness of theleft eye in centring abduction movements; thiswas exacerbated with head turned to the left.With head turned to the right, the right eye de-veloped a decentring abduction weakness and theleft eye, a further adduction weakness (Fig. 2).With head turned to the right there was also anobservable first degree nystagmus of the right eyewhich rebounded.

Head Primary

/ ~~~~~~30"RR -\ Primary

Head Right~~~~30~RA A A

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-"",~~PFig. 2 Decentring and centring eye movemtenttsexecuted between primary gaze (P) and a target 300right. Subject 2 of group 2. R=right eye; L=left eye;arrowheads-saccades of nystagmus. With headrotated to right the right eye makes an abnormalabduction movement, which can be compared withthe normal abduction made by the right eye in thehead primary position, and hav a first degreenystagmus.

Subject 3-female, 22 years old. Eye movementsin all head positions were within the normal rangewith one exception. With head turned to the rightthere was a centring abduction weakness of theleft eye (Fig. 3). This finding was repeatable, andthe low velocity of the saccade was statisticallysignificant.

GROUP 3 EFFECTS OF HEAD TURNING ON SACCADICEYE MOVEMENTS IN MULTIPLE SCLEROSISMeasurements of peak velocities of saccadic eyemovements are presented in Table 3. The tableshows that patients 2 and 5 had weakness of sac-cadic eye movement when tested with the head inits primary position. Four patients had weakness

M. Gresty

Head Primary

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L

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100 msFig. 3 Decentring and centring eye movementsexecuted between primary gaze (P) and a target 300right. Subject 3 of group 2. R =right eye; L=left eye.The left eye has a weakness of centring abduction inthe head right position. All other saccades are normal.

of saccadic movements when the head was turnedlaterally. Head turning had no effect on onepatient. This disorder revealed by head turningin these patients was predominantly a weaknessof abduction.The head turning test doubled the incidence of

detection of abnormal saccades in this group ofpatients. It is noteworthy that no evidence ofanterior internuclear ophthalmoplegia was re-vealed by the test.

GROUP 4 DISORDERS OF EYE MOVEMENT REVEALEDBY HEAD TURNING IN PATIENTS WITH DOWNBEATNYSTAGMUSFour patients presenting in common the symptomof downbeat nystagmus and suffering from avariety of neurological diseases were selected forthis study. The statistics relating to peak saccadicvelocities are presented in Table 4. In all patients,head turning revealed further defects of eye move-ment. Again, the pattern of disorder revealed byhead turning has to be considered in respect ofeach individual patient and no generalisations canbe made. Head turning showed weakness of ab-duction or adduction in almost equal numbers.



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Clinical observation had revealed no disconjuga-tion of eye movement in these patients.

Patient 1, a 36 year old female, presented witha predominantly left sided cerebellar syndromeand brain stem signs. Neurological examinationrevealed gait ataxia, increased tone in all fourlimbs, and exaggerated reflexes. Tomograms ofthe foramen magnum showed backward deformityof the odontoid process encroaching upon theforamen magnum. There was an anomaly of thearch of the atlas. A myelogram showed signsof cervical syringomyelia with cerebellar ecto-pia associated with arachnoiditis and vascularproliferation.Saccadic eye movements:Head primary-shape and velocity were found to

be within normal limits.Head turned to left-there was bilateral weakness

of adduction and abduction.Head turned to right-there was adduction weak-

ness of the right eye and adduction and abduc-tion weaknesses of the left.Patient 2, a 73 year old female, presented with

predominantly left sided cerebellar signs, poorconvergence, and impaired vibration sense. Thelesions were probably widespread and vascular innature.Saccadic eye movements:Head primary-the shape and velocity were found

to be within normal limits.Head turned to left-there was bilateral weakness

of abduction.Head turned to right-movements were withinnormal limits.Patient 3, a 39 year old male, presented with

multiple brain stem and cerebellar signs in theform of gait ataxia and weakness of the legs,exaggerated tendon jerks, extensor plantar re-sponses, and clumsiness of the right hand.Necropsy showed an Arnold Chiari type 1 malfor-mation. The right cerebellar tonsil extended acrossthe midline and was larger than the left; theyextended caudally to 15 mm below the level of thearch of the axis. The medulla oblongata waselongated.Saccadic eye movements:Head primary-abduction weakness was present

in the left eye.Head turned to left-there was abduction and ad-

duction weakness in the right eye.Head turned to right-there was abduction weak-

ness and improved left eye abduction.Head turning to the left revealed right eye weak-ness and improved left eye abduction.

Patient 4, a 45 year old male, presented with a

cerebellovestibular syndrome of seven years' dura-tion believed to be familial cerebellar degenera-tion. (The earliest sign to appear was downbeatnystagmus).Saccadic eye movements:Head primary-bilateral abduction weakness was

present. The left eye adduction was weak.Head turned to left-there was bilateral abductionand adduction weakness.

Head turned to right-there was bilateral abduc-tion and adduction weakness.

COMMENT UPON SIGNIFICANCE OF TESTOn the sole basis of measurements of peak saccadicvelocity, taking mean velocities of less than 320°/sas significant, head turning quadrupled the inci-dence of abduction weakness and increased theincidence of adduction weakness tenfold.

Discussion

IMPLICATIONS OF FINDING LATENT DISORDERS OFEYE MOVEMENT IN NORMAL SUBJECTSThe study demonstrates clearly that subjects withno neurological complaints can be shown to have'latent' disorders of eye movement. There are twointerpretations of this finding. Either the disordersmerely represent the extremes of the normal rangeof behaviour or they are subclinical evidence ofpathological lesions of the nervous system. Thelatter interpretation is favoured for severalreasons. The abnormal eye movements revealedby head turning were not variations of the normalpatterns but were often quite different in shapeand associated with distinctly abnormal signs suchas unilateral nystagmus. Furthermore, an abnor-mality of movement could be revealed in a specifichead position; the same movement in the othertwo head positions was normal, and the character-istics of the movements did not appear to lie onthe same statistical continuum. Finally, the peakvelocity criterion adopted for the experiment wasdeliberately set very low, much lower than thecriterion used for clinical testing in our own andin many other ENT laboratories.

If the conclusion is true that the test revealslesions of the nervous system, it may be a sensitiveindicator of susceptibility to vascular or degenera-tive disease.

POSSIBLE MECHANISMS BY WHICH HEAD TURNINGREVEALS EYE MOVEMENT DISORDERSMechanical deformation of the brain or its vas-cular supply may alter the activity of nervoustissue by reducing local blood supply, therebyrendering the tissue anoxic. In addition, it is pos-

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sible that stretching or compression of nervoustissue can change the electrical characteristics ofaction potentials, rendering saltatory conductionless secure, in a way similar to the effect of heaton demyelinated peripheral nerve (Rasminsky,1973). Either or both of these mechanisms may beoperating in subjects with latent disorders of eyemovement.The patterns of abnormal movement revealed in

normal subjects show most clearly how thesemechanisms might operate. Subject 2 of group 2showed several abnormalities of eye movementwhen the head was turned to the right. Theseincluded weak abduction of the right eye, adduc-tion weakness of the left and a rebound nystagmuson right gaze. All these abnormalities are explic-able if one assumes a degraded function of theright side of the brain stem and cerebellum. Thedegradation could arise if head turning to theright restricted flow through the right vertebralartery without adequate compensation from otherblood vessels. For this state to occur it mustbe assumed that this person has vascularabnormalities.

In contrast, subject 3 of group 2 exhibited anisolated weakness of centring abduction in onlyone head position. To explain this it must beassumed that in the locality of the left abducensnucleus or of the neurones which inhibit the ipsi-lateral medial rectus motor neurones, localmechanical forces either restrict the vascularsupply to these neurones or change their trans-mission characteristics. Again, an inherent defectis implicated.

In patients with multiple sclerosis there is theobvious possibility that mechanical deformationreveals functional defects in nervous tissue whichis susceptible to stress because of demyelination.McAlpine et al. (1972) imply that head turningmay be used to differentiate between multiplesclerosis and vertebrobasilar ischaemia becausethe head turning exacerbates the symptoms byincreasing the extent of the ischaemia. However,ocular defects were revealed by head turning inthe group of young people with multiple sclerosisin whom there was no evidence or likelihood of avascular disorder. Our conclusion is that headturning can exacerbate disorders of oculomotorfunction in both multiple sclerosis and vasculardiseases but is not an efficient test for differentialdiagnosis between them.

Patients with malformations in the region ofthe foramen magnum are most likely to have ab-normalities of eye movement produced by vascularderangement because of the experimental demon-

M. Gresty

stration that, in injuries which compress structurespassing through the foramen magnum, the vascu-lature is first, and nervous tissue last, to suffer(Taylor and Byrnes, 1974).We have no convincing explanation for abnor-

mal eye movements produced by head turning inpatients with cerebellar degeneration. Such apatient reported in this study (patient 4, group 4)had a massive loss of cerebellar volume. Thiscould allow unusually large movements of thebrain stem during head turning. However, thetest is now used routinely in our laboratory, andrecently it has revealed abnormalities of conjugategaze in a patient with minimal atrophy of theposterior vermis of the cerebellum.

NERVOUS MECHANISMS OF DISCONJUGATE EYEMOVEMENTS

The most common defect this study encounteredwas an abduction weakness, even in the group ofpatients with multiple sclerosis. In particular,centring abduction was often found to be weakwhen decentring was normal. The abducensnucleus being the most caudally placed of alloculomotor nuclei is most likely to be affectedby twisting the brain stem which would explainthe high incidence of abducens weakness.

Abduction may be weak because firing rates inthe sixth cranial nerve are low; alternatively, anapparent weakness may be seen because the ipsi-lateral medial rectus is not fully relaxed. Thiscould result from a reduction of the inhibitoryinput to medial rectus motor neurones, which isapplied during abduction (Maeda et al., 1972). Itis believed that the inhibitory pathway to the ipsi-lateral medial rectus originates from about thelevel of the abducens nucleus and travels in thecontralateral medial longitudinal fasciculus (Polaand Robinson, 1976) and, furthermore, that in thevicinity of the abducens nucleus are neuroneswhich are responsible for conjugate lateral gaze(para-abducens nucleus). Their axons cross to thecontralateral medial longitudinal fasciculus andmake excitatory synapses with the contralateralmedial rectus motor neurones (Carpenter andMcMasters, 1963; Carpenter et al., 1963; Bakerand Highstein, 1975). Robinson (1970 has pro-posed that anterior internuclear ophthalmoplegiais caused by a lesion in the medial longitudinalfasciculus which affects both the inhibitory inputto the ipsilateral medial rectus neurones and theexcitatory input to the contralateral medial rectus.The lack of inhibition to the ipsilateral medialrectus means that abduction in this eye should beslower than normal and this has been demon-



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strated physiologically by Loeffler et al. (1966) andbehaviourally by Bird and Leech (1976).

If it is assumed that a lesion can affect only theinhibitory pathway to the ipsilateral medial rectus,only abduction in that eye will be slowed, as inmany of our subjects. This may be one mechanismof posterior internuclear ophthalmoplegia.

Finally, an explanation may be offered for thefact that centring abduction is often weak whendecentring appears normal. During adduction allabducens neurones are inhibited (Fuchs andLuschei, 1970). In contrast, during abduction,medial rectus motor neurones may continue firing(Robinson, 1970). The number and firing rates ofoculomotor neurones increase in proportion to eyedisplacement in the 'on' direction (Schiller, 1970).Hence if the eye begins to abduct from a nasalposition in which fewest motor units are recruited,and inhibition is reduced on the antagonist motorneurones, the abduction will be reduced in itseffectiveness.

Conclusion

The simple geometry of the eye and the ease ofelectro-oculographic recording enable precisequantitative descriptions of oculomotor functionto be given. As a consequence, eye movement testsare very sensitive indicators of neurologicaldiseases.

It has been demonstrated that when eye move-ment tests are carried out with the head placedin eccentric positions, disorders of eye movementare recorded which are not apparent on conven-tional testing. In particular, disorders of conjugategaze occur. These 'latent' defects of eye move-ment appear because, when the head is turned,there are differential compression and stretchingeffects on the vertebral arteries which may leadto local or generalised vertebro-basilar ischaemiaif the vasculature is inherently defective.Head turning reveals disorders of conjugate

gaze, particularly in patients with suspected lesionsof the low brain stem and cerebellum. The testalso increases the incidence of dissociation of gazein patients with multiple sclerosis. In this disease,two hypotheses to explain the effect of head turn-ing are tenable. Either local restrictions of bloodsupply exacerbate faulty transmission in diseasednervous tissue or the mechanical stretching andcompression on nerves, which result directly fromtwisting the brain stem, adversely affect themechanisms of transmission.The most common finding in patients with mul-

tiple sclerosis is a weakness of abduction. This can

be explained by the hypothesis that there is alesion of the inhibitory pathway to the ipsilateralmedial rectus muscle (antagonist of the abduc-tion). This hypothesis unifies the explanations ofposterior and anterior internuclear ophthalmo-plegia and distinguishes them as functional ratherthan anatomical entities.The head turning test reveals defects of eye

movement in otherwise healthy young people andthus may be a sensitive indicator of inherentskeletal and vascular defects.

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Eccentric head positions reveal disorders of conjugate · JournalofNeurology, Neurosurgery, andPsychiatry, 1977, 40, 992-1002 Eccentric headpositions reveal disorders ofconjugate