Past-Pointing in Paralytic Strabismus

Past-Pointing in Paralytic Strabismus

PAST-POINTING IN PARALYTIC STRABISMUS GUNTER K . VON NOORDEN, M . D . , SHINOBU A W A Y A , M . D . , AND P A U L E . ROMANO, M . D . Baltimore, Ma...

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PAST-POINTING IN PARALYTIC

STRABISMUS

GUNTER K . VON NOORDEN, M . D . , SHINOBU A W A Y A , M . D . , AND P A U L E . ROMANO, M . D .

Baltimore, Maryland Anomalies of egocentric localization were first described by von Graefe in patients with recent paralyses of the extraocular muscles and are referred to as "past-pointing" or "false orientation." If the patient, while his sound eye is covered, is asked to point toward an object located in the field of action of the paretic muscle, his finger will point beyond the object and towards the field of action of the paretic muscle. 1

According to von Helmholtz, Bielschowsky, and Hof mann egocentric localization of visual objects in subjective space is almost accurate as long as there is proper correlation between ocular innervation and its effect—i.e., as long as the amount of actual eye movement corresponds to what is intended. In the case of a left abducens paralysis, for example, this correlation is no longer correct. When the object lies to the left of the patient, an abduction impulse will be given but the eye moves little or not at all. The patient will judge the position of the object as being to the left of its actual location, and he will past-point to the left. 2

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is thus imaged on nasal retinal points and therefore is localized temporally : the patient will past-point temporal to the object he is fixating. According to this theory the distance between the fovea and the eccentric retinal elements on which the image is falling determines the angle of past-pointing. Adler noted that when foveal fixation was enforced by having the patient fixate a foveal target positioned in the field of gaze of the paretic muscle, past-pointing was absent. The view that past-pointing is determined by the position of the image on the retina has been supported by Goswami, Bedrossian, and Walsh and Hoyt. 6

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A third theory of past pointing is based on the discovery of sensory receptors in the extraocular muscles. Their existence has led many investigators to believe that there is proprioceptive feedback from the extraocular muscles to the central nervous system that influences egocentric localization of objects (Tschermak and Oppel ). Thus, pastpointing is felt to be caused by a disparity between the information received by the brain from the extraocular muscles and the amount of motor impulses required to produce adequate movement into the field of action of a paretic muscle. This view was most recently expressed by Lyle and Wybar and the Hugonniers in their textbooks on strabismus. 9

This classical theory of Helmholtz, Bielschowsky, and Hofmann has not remained unchallenged, and in 1945 another explanation of past-pointing was proposed by Adler. That author believed that the paretic eye cannot be moved sufficiently to permit fixation of an object with the fovea when looking into the direction of a paretic muscle. In the case of an abducens paralysis the object 5

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Stimulated by this discrepancy of opinion regarding the mechanism of a frequently observed clinical phenomenon, we have studied egocentric localization in normal subjects and in patients with paretic strabismus of recent onset.

From the Wilmer Institute of Ophthalmology, The Johns Hopkins University School of Medicine and Hospital, Baltimore, Maryland. Supported by Research Grant EY-00274 from the National Eye Institute. This paper was presented before the 106th meeting of the American Ophthalmological Society, May 27, 1970, Hot Springs, Virginia. Reprint requests to Gunter K. von Noorden, M.D., The Wilmer Institute, The Johns Hopkins University School of Medicine and Hospital, Baltimore, Maryland 21205.

MATERIAL AND METHODS

A method was used that had in principle already been employed by von Graefe and consisted of a quantitative comparison of the 1

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position of a visual object as it appears to the patient with its objective location. A hemicylindrical translucent screen was mounted on a horizontal wooden plate. The patient faced the center of this screen; his head was stabilized by a bite-board ( Fig. 1 ) . Only one eye was tested at a time, and the eye not to be tested was occluded. Electric light bulbs were attached to the back of the screen in different positions and were operated from a switchboard. A soldering gun had been modified by building a light projector into the barrel of the pistol ; pulling the trigger activated the projector. The pistol was held by the patient; the arm with the pistol remained under the table so that the patient was unable to correct visually for errors of localization. Alerted by a verbal signal, the patient's task was to extend his arm forward and to "shoot" at lights appearing at eye level in his median plane, and at 30° to the right and to the left. After each test, the arm had to be rested in the lap for 30 seconds to avoid proprioceptive memory of its previous position. The position of the projected light was noted by the examiner from the back of the screen, and errors of localization were recorded. Each session consisted of 25 measurements in each of the different positions of gaze. These pointing tests were repeated on three different days in nine normal subjects with right-eye dominance and right-handedness. Two patients with left abducens paralysis were tested only on one occasion. Three subjects were also tested with the eyes in positions of extreme abduction ( 6 0 ° ) , and the fixation behavior was determined with a vertical afterimage produced on the fovea in these subjects and in one patient (Case 2) with abducens paralysis. After the afterimage was elicited with an electronic flash immediately following each pointing experiment, the patient identified the position of the afterimage with a hand-held projector while fixating on each of the fixation lights. Superimposition of the afterimage on the fixation light indicated foveal fixation;

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Fig. 1 (von Noorden, Awaya, and Romano). Pointing experiment to determine egocentric localization of visual objects. For details, see text.

inability to superimpose the afterimage on the light indicated eccentric viewing. For instance, with the right eye abducted, projection of the afterimage 10° to the left of the light indicated that the image of the fixation light was positioned 10° nasal to the fovea. RESULTS

The results of pointing experiments in a normal right-handed and right-eyed subject is shown in Figure 2. The data are presented as a frequency distribution of errors of localization and are superimposed on the normal limit of errors (shaded portion) calculated with ± 2 standard deviations from the mean of errors of each of the nine normal subjects. The results show that haptic localization of visual targets positioned at 0° and at 30° to the right was quite precise when viewed with the left eye. However, when looking with either eye at a light 30° to the left, and with the right eye at a light at 0°, slight past-pointing to the right occurred. This slight shift to the right was also noted when localizing with the dominant right eye to the left and at 0° in the majority of the other normal observers. This tendency is reflected in the distribution of mean errors in this position. Next, we established that the precision of localization is not influenced by the position

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PAST-POINTING IN PARALYTIC STRABISMUS O.B

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Fig. 2 (von Noorden, Awaya, and Romano). Subjective localization of visual targets presented 30° to the left, in the objective median plane, and 30° to the right of a normal, right-handed and right-eyed subject. Left: right eye open. Right: left eye open. Abscissa indicates the errors of localization in degrees; the ordinate, the number of localizations; the arrow, the arithmetic mean of errors.

of the image on the retina. When a normal subject views a visual object in extreme positions of gaze, the image no longer falls on the fovea but on eccentric retinal elements, i.e., the visual objects are now viewed in a secondary rather than in the principal visual direction. Pointing experiments performed in a normal subject (Fig. 3) revealed that localization of visual targets in the extreme lateral periphery of the visual field ( 6 0 ° ) remained essentially correct even though foveal fixation could no longer be maintained in this position. A foveal afterimage was projected 10° to the right of a fixation light positioned 60° to the left when viewed with the left eye, and 10° to the left when the target was 60° to the right and viewed with the right eye, respectively. This indicated that the image of the fixation light was formed eccentrically and 10° nasal to the fovea of each eye in each instance. Yet, no past-pointing occurred under these conditions. This experiment was repeated with identical results in two other normal subjects. Thus, the accuracy of localization does not depend on whether visualized objects are viewed by the subject foveally or with peripheral retinal elements. Two patients with paresis of the left abducens nerve were examined in a similar manner.

CASE REPORTS

Case 1—This 12-year-old boy (A.J.) was struck by a truck six months prior to examination and has seen double in the left field of gaze since the injury. Visual acuity : 20/20 with each eye. Ductions : moderate limitation of abduction, R E ; however, the eye can be moved at least 15° towards abduction from the primary position. Case 2—This 51-year-old woman (H.D.) noted a sudden onset of diplopia accompanied by nausea and dizziness one week prior to the test. Visual acuity : 20/20 with each eye. Ductions : moderate limitation of abduction, RE, but movement of the paretic eye considerably beyond the midline is possible (Fig. 4).

The results obtained from these two patients are shown in Figures 5 and 6. Figure 5 shows past-pointing with the paretic eye to the left not only in the field of action of the paretic muscle but also in primary position and, to a lesser degree, in adduction. Shortpointing to the right (spastic localization) occurred when the normal right eye was fixating in adduction. Similar findings were obtained in the second case. Marked pastpointing occurred in the direction of the paretic field of gaze, and was present to lesser degrees in primary position and adduction. When fixating with the sound right eye a tendency to past point to the right was observed. In this patient a foveal afterimage was employed in order to control the fixation behavior. The position of the afterimage in abduction indicates eccentric viewing of the

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fixation light : its image fell on nasal retinal elements, 10° off the fovea. However, this can hardly be the cause of past-pointing, since a significant localization error occurred also in primary position and in adduction where the position of the afterimage clearly indicated foveal fixation. DISCUSSION

Past-pointing is a clinical phenomenon of limited diagnostic value but of considerable theoretical interest. It occurs in extraocular muscle paralyses and pareses of recent onset, and it usually disappears after several weeks but has been observed by us as long as five years after onset of the paralysis. Our findings in normal subjects show that hap tic localization of a visual stimulus is approximately correct even when visual control

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of the pointing hand is excluded. The range of localization errors was small. It is of interest, however, that all the normal subjects who were right-handed and right-eye dominant made a small but consistent pointing error to the right when fixating with the right eye on a target positioned in the median plane and 30° to the left. This observation differs from the results of pointing experiments reported by Stiefbold, who noted slight degrees of past-pointing to the left when normal right-eyed and right-handed subjects were tested in primary position. It appears that ocular dominance and handedness, and perhaps some unknown factors, may influence the correctness of egocentric localization, and these consistent variations observed in normals warrant further investigation. 13

Lateral and Extreme (approx. 6 0 ° ) Lateral Gaze

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Fig. 3 (von Noorden, Awaya, and Romano). Subjective localization, in normal subjects, of visual targets located 30° to the right and left of the median plane (position of afterimage indicates foveal fixation) and 60° to the right and left of the median plane (position of afterimage indicates viewing with retinal elements 10° nasal to fovea).

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Our data from patients with abducens pareses provide evidence contrary to the widely held view that the angle of past-pointing is determined by the eccentric position of the image on the retina. An image displacement may well occur in the field of action of the paretic muscle and would be caused by inability to move the paretic eye far enough to position the image on the fovea. However, as shown in our patients, past-pointing occurs not only in the field of action of the paretic muscle but also in primary position and adduction, where superimposition of a foveal afterimage on the fixation light clearly indicated foveal fixation. Past-pointing did, in fact, also occur in the nonparetic eye of one patient in whom spastic localization was observed in adduction. 14

There is, in our opinion, no reason to postulate that an extrafoveal position of a retinal image leads to errors of egocentric localization. The fact that an image on the nasal retina is localized in the temporal visual field does not imply that the object cannot be localized correctly in reference to the patient's egocenter. Our findings in normal subjects show that visual objects in the extreme lateral periphery can no longer, as one would expect, be aligned with the fovea. Yet, localization of these visual objects was as precise as during foveal fixation when they were positioned within the range of normal ocular motility.

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Fig. 4 (von Noorden, Awaya, and Romano). Case 2. Top: Esotropia in primary position. Bottom : Left abducens paresis in levoversion.

Past-pointing is an error of egocentric localization which pertains to optic localization of visual objects in their relation to the observer's body and the observer's tactile, visual, and conceptual image of his body position. Egocentric localization of objects in space is approximately correct as long as there is no discrepancy between the innervational input to move the eyes into a certain direction and the amplitude of the actual movement. In left abducens paresis, for instance, excessive innervational impulses are required to move the left eye into abduction, and are required to counteract the unopposed antagonistic medial rectus muscle when holding the eye in primary position. Thus, the subjective impression is created that the object to be fixated lies to the left of the me14

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Fig. S (von Noorden, Awaya, and Romano). Case 1. Subjective localization in patient with left abducens paresis. Left: RE fixating. Right: LE fixating. For explanation, see text.

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Fig. 6 (von Noorden, Awaya, and Romano). Case 2. Subjective localization by patient with left abducens paresis. Left: RE fixating. Right: LE fixating. Foveal afterimage indicates foveal fixation in primary position and adduction. Note the past-pointing in these positions when the paretic eye was fixating.

dian plane. Short-pointing in adduction that was observed in both of our patients may be explained on a similar basis: Since the medial rectus muscle is unopposed by its paretic antagonist, less than normal innervation is required to adduct the eye. Consequently, the object will be localized to the left of its actual position. On the basis of our findings we believe that the classical theory of past-pointing, as an error of egocentric localization caused by disproportion between motor innervation and its effect, still holds true today. Also, the view that misinterpretation of proprioceptive feedback from the extraocular muscles may give rise to past-pointing must be rejected because at present there is no evidence whatever of proprioception from sensory receptors in the extraocular muscles. " Whether or not the muscle spindles, whose présense in human extraocular muscles has been known for almost 100 years, serve any function is speculative. 15

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SUMMARY

Clinical experiments in normal subjects and patients with paralytic strabismus revealed that past-pointing may occur despite foveal fixation, that it may be absent even though the

image of the fixated object falls on peripheral retina, that it may occur not only in the paretic, but also in the nonparetic field of gaze, and even in the nonparetic eye. These results support the classic theory of past-pointing as an error of egocentric localization and refute the more modern attempts to explain this phenomenon on the basis of the position of the image on the retina.

REFERENCES

1. von Graefe, A.: Beiträge zur Physiologie und Pathologie der schiefen Augenmuskeln. Graefe's Arch. Ophth. 1:1-81, 1854. 2. von Helmholtz, H.: Helmholtz's Treatise on Physiological Optics (J. P. C. Southall, trans.). New York, Dover Publications, 1962, vol. 3, chap. 29. 3. Bielschowsky, A. : Die Motilitaetsstoerungen der Augen. In Graefe, A., and Saemisch, T. (eds.) : Handbuch der gesamten Augenheilkunde, 2nd ed. Berlin, J. Springer, 1939, vol. 8, chap. 11. 4. Hofmann, F. B. : Die Lehre vom Raumsinn. In Graefe, A., and Saemisch, T. (eds.) : Handbuch der gesamten Augenheilkunde, 2nd ed. Berlin, J. Springer, 1925, vol. 3, chap. 13. 5. Adler, F. H. : Pathologie physiology of convergent Strabismus. Motor aspects of the nonaccommodational type. Arch. Ophth. 33:362, 1945. 6. Goswami, A. P. : A theory for false projection. Acta Ophth. 4 5 :699, 1967. 7. Bedrossian, E. H. : The Surgical and Nonsurgical Management of Strabismus. Springfield, Illinois, Charles C Thomas, 1969, p. 125.

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8. Walsh, F. B., and Hoyt, W . F. : Clinical Neuro-ophthalmology, 3rd ed. Baltimore, Williams and Wilkins, 1969, vol. 1, p. 147. 9. von Tschermak-Seysenegg, A. : An Introduction to Physiological Optics (P. Boeder, trans.). Springfield, Illinois, Charles C Thomas, 1952, p. 219. 10. Oppel, C. : On the motor, sensorial, and sensible nervous apparatus in human eye muscles and their significance for sensorial physiology. Graefe's Arch. Ophth. 171:337, 1967. 11. Lyle, T. K., and Wybar, K. C : Practical Orthoptics in the Treatment of Squint (and Other Anomalies of Binocular Vision), 5th ed. Springfield, Illinois, Charles C Thomas, 1967, p. 619. 12. Hugonnier, R., and Clayette-Hugonnier, S.: Strabismus, Heterophoria, Ocular Motor Paralysis. Clinical Ocular Muscle Imbalance (S. Veronneau-

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Troutman, trans.). St. Louis, Mosby, 1969, p. 269. 13. Stiefbold, U.: Untersuchungen über Beziehungen zwischen der haptischen und optischen Lokalisation. Dissertation, University of Tübingen Medical School, 1964. 14. Bielschowsky, A. : Lectures on Motor Anomalies. Hanover, Dartmouth Publications, 1940, p. 65. 15. Irvine, S. R., and Ludvigh, E. J.: Is ocular proprioceptive sense concerned in vision? Arch. Ophth. 15:1037, 1936. 16. Christman, E. H., and Kupfer, C. : Proprioception in extraocular muscle. Arch. Ophth. 69 : 824, 1963. 17. Merton, P. A. : Absence of conscious position in the human eyes. In Bender, M. B. (ed.) : The Oculomotor System. New York, Harper & Row, Hoeber Medical Division, 1964, chap. 14, p. 314.