- Email: [email protected]
Abnormalities of the Vestibulo-Ocular Response in Congenital Esotropia
ABNORMALITIES OF T H E VESTIBULO-OCULAR RESPONSE IN CONGENITAL ESOTROPIA C R E I G S. H O Y T ,
M.D.
San Francisco, California
In 32 infants with congenital esotropia, I measured the vestíbuloocular response. The eight patients with nystagmus compensation syndrome exhibited brisk responses. Fourteen of the 24 who had esotropia without nystagmus had severely diminished responses and the other ten had moderate responses. Vestíbulo-ocular testing is useful in detecting subtle forms of nystagmus compensation syndrome, especially in young infants, in whom thorough examination of auctions and versions is difficult. Dysfunction of the vestibular system is not necessarily a primary cause of congenital esotropia, but brain-stem function in patients with congenital esotropia should be studied further.
When a full-term neonate is held at arms' length under the axillae, with his head tilted forward 30 degrees, and is rotated, his eyes deviate in the direction toward which the examiner is rotating the eye realignment, away from the direction of rotation. This vestibulo-ocular response induced by head movement produces a slow eye movement opposed to the infant's head movement, which decreases movement of the images on the retina. The slow components of the vestibulo-ocular response and optokinetic movement take place in the same direction and act synergistically to match the velocity of the head movement and more effectively stabilize the retinal images, thus improving vision. I found a consistent abnormality of the vestibulo-ocular response in infants with congenital esotropia that easily distin1
Accepted for publication Feb. 24, 1982. From the Departments of Ophthalmology and Pediatrics, University of California Medical Center, San Francisco, California. Reprint requests to Creig S. Hoyt, M.D., Room A-751, University of California, San Francisco, CA 94143. 704
guishes these children from those with nystagmus compensation syndrome. 2
SUBJECTS AND METHODS
I studied the vestibulo-ocular responses in 32 consecutive infants referred here with the diagnosis of congenital esotropia from February 1980 to October 1981. All of these patients had (1) onset of esotropia before the age of 6 months, documented by at least one examining ophthalmologist, (2) nonaccommodative esotropia present at all times and relatively stable in size of deviation, and (3) no known ocular or central nervous system disease other than abduction nystagmus. I considered children with esotropia and abduction nystagmus to have nystagmus compensation syndrome if they met the criteria outlined by von Noorden : (1) onset of esotropia in early infancy, (2) pseudoparesis of both abducens nerves, (3) head turn toward the side of the fixing eye, (4) absence of nystagmus with the fixing eye in adduction, and (5) appearance of a manifest jerk nystagmus as the fixing eye moved into primary position 2
© AMERICAN JOURNAL OF OPHTHALMOLOGY 93:704-708, 1982
VOL. 93, NO. 6
VESTIBULO-OCULAR RESPONSE IN ESOTROPIA
705
and abduction. Eight of the 32 infants vestibular stimulation, especially in the met these criteria. abducting eye. The other ten had a reI tested all the infants by standard sponse of 1 + in the fast phase. None of techniques of measuring the angle of stra- the patients with nystagmus compensabismus with the prism and cover test on tion syndrome exhibited a depressed ocuan accommodative target at 33 cm and on lar response to vestibular stimulation, a fixation light at 6 m. I analyzed the and none of the patients with congenital ductions and versions using various mov- esotropia demonstrated a brisk ocular reing fixation targets. I completed a cyclo- sponse. plegic refraction after instilling 1% atroDISCUSSION pine in both eyes of the infants on three consecutive days. The vestibular system is unique among Vestibular stimulation of the infants oculomotor subsystems because of its was provided by rotation. I held the rapid maturation in neonates. The vestibinfants vertically and facing me, with my ular system is anatomically complete and hands surrounding the infant's trunk. The functionally responsive at or before infant's head was bent forward 30 degrees birth. Newborn, full-term infants reover the body. Rotation of the infant 360 spond to acceleration. Their eyes deviate degrees around the examiner's axis pro- in the expected direction of the slow duced deviation of the eyes and head component, although acquisition of the opposite to the direction of rotation. A fast component with its probable pontine fast, recorrection ocular movement in the origin may be delayed in premature indirection of rotation represented the fants or those who are small for their other phase of the induced vestibulo- gestational age. " Children who have sufocular response. I graded this fast phase fered perinatal insults to the central nervas follows: 0 if no more than two to three ous system frequently fail to acquire this beats were seen with a single 360-degree fast component. rotation, 1 + if four to ten beats occurred, Vestibular dysfunction including alteraand 2 + if more than ten beats resulted tions in the vestibular ocular response from a single rotation. Normal, nonstra- reportedly occurs frequently in children bismic children usually exhibit a 2 + re- with various disorders involving minor sponse after the age of 1 month. I graded neurologic impairment. ' Abnormal ocuthe vestibulo-ocular response during ro- lar responses to vestibular stimulation tation, not upon completion of rotation. I have been reported in patients with strarotated the infants both clockwise and bismus. Doden and Adams described counterclockwise, paying special atten- involuntary, rhythmic, conjugate, pendution to the response of the abducting eye. lar deviations on vestibular testing of 23% of 150 patients with various forms of RESULTS strabismus. Salman and von Noorden The vestibulo-ocular responses of the reported a number of abnormal responses 32 infants are summarized in Tables 1 and to caloric stimulation in strabismic chil2. All eight patients with nystagmus com- dren, including postcaloric nystagmus of pensation syndrome demonstrated a irregular amplitude and frequency, vesbrisk ocular response to rotation. Four- tibular hyperexcitability, and irregular teen of the 24 patients with congenital eye movements with the eyes closed at esotropia without nystagmus demon- rest. Their report made no specific menstrated little or no fast ocular phase to tion of any abnormality of the vestibular 3
4
6
7 10
11,12
11
12
706
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1982
TABLE 1 CLINICAL FINDINGS IN C H I L D R E N W I T H CONGENITAL ESOTROPIA
Patient No., Sex, Age at First Examination (mos) 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24,
M, M, F, M, F, F, F, M, M, M, F, M, M, F, F, M, F, M, M, M, F, F, M, F,
3 7 11 6 16 4 9 8 4 2 6 5 5 2 8 29 4 5 3 6 8 5 11 4
Near
Distance
Fast Phase of Vestibulo-ocular Response*
55 60 45 70 60 50 60 60 60 55 40 65 60 55 70 65 50 30 65 45 60 70 55 70
55 60 45 70 60 50 60 60 50 55 40 65 60 55 60 65 50 30 65 45 60 70 57 70
0 1+ 0 1+ 0 0 1+ 1+ 0 1+ 1+ 0 0 0 1+ 1+ 0 0 0 0 1+ 0 1+ 0
Initial Deviation (Prism Diopters)
* Grading system: 0 = 2 to 3 beats/360-degree rotation; 1+ = 4 to 10 beats; and 2 + = more than 10 beats.
response in infants with congenital esotropia. Although the term "congenital esotropia" is well established, it is misleading. Newborns rarely have a constant, large-
angle esotropia; indeed, their eyes either are exotropic or exhibit a skew deviation. Therefore, neonatal esotropia might more correctly describe this earlyonset esotropia that presumably occurs 13
14
TABLE 2 CLINICAL FINDINGS IN C H I L D R E N W I T H NYSTAGMUS COMPENSATION SYNDROME
Patient No., Sex, Age at First Examination (mos) 1, 2, 3, 4, 5, 6, 7. 8,
M, M, F, M, F, M, F, M,
6 11 20 5 3 10 6 8
Near
Distance
Fast Phase of Vestibulo-ocular Response*
60 70 70 45 60 55 60 70
60 70 70 40 60 55 60 70
2+ 2+ 2+ 2+ 2+ 2+ 2+ 2+
Initial Deviation (Prism Diopters)
'Grading system: 0 = 2 to 3 beats/360-degree rotation; 1+ = 4 to 10 beats; and 2 + = more than 10 beats.
VOL.
93,
NO.
VESTIBULO-OCULAR RESPONSE IN ESOTROPIA
6
before the normal establishment of binocular reflexes. However, I use the term congenital rather than neonatal esotropia because it has been so well established. This condition is probably not the result of hyperopia or excessive accommodative effort, although the essentially nonaccommodative origin of congenital esotropia has been challenged. It is unlikely that injury to the abducens nerve is a primary cause of this disorder even in those patients with esotropia and abducting nystagmus. The specific factors that cause congenital esotropia remain to be defined, although a large number of affected patients show other overt signs of central nervous system dysfunction. Mitsui and colleagues' recent electromyographic study of patients with esotropia demonstrated that in some cases the medial recti muscles continued to fire tonically while the patient was under general anesthesia. When retrobulbar anesthesia was superimposed on one eye, the discharge from the ipsilateral medial rectus muscle decreased. However, this decrease was accompanied by a reciprocal increase in the discharge from the contralateral medial rectus muscle. Mitsui and associates suggested that this reciprocity could be explained by blockage of unilateral proprioception by the retrobulbar anesthesia. They did not know what factors might cause an abnormal excitation of proprioceptive impulses from extraocular muscles. However, their results suggest that the medial recti muscles are tonically driven by a neural system that is unaffected by general anesthesia. In light of this finding, it is not surprising that the duration of the fast phase of the vestibulo-ocular response, especially in the abducting eye, is attenuated in congenitally esotropic patients. Objective documentation of this abnormal vestibulo-ocular response is desirable, but it is difficult to record ocular move15
16
17
18
19
20
707
ment objectively in infants. The results of my study do not prove that congenital esotropia may be the result of damage to or miswiring of the vestibular ocular motor system. However, neonatal skew deviation may precede classic congenital esotropia, which supports vestibular dysfunction as a possible cause of congenital esotropia. Currently, vestibulo-ocular testing of congenitally esotropic patients is useful regardless of what it may indicate about the cause of this disorder. Overt cases of nystagmus compensation syndrome can be recognized easily, but subtle forms of the syndrome are easily overlooked. Moreover, the long-term prognosis for establishing a stable ocular alignment appears to be poorer in patients with nystagmus compensation syndrome than in those with esotropia without nystagmus. The recognition of subtle forms of the syndrome is, therefore, therapeutically and prognostically important. Finding an enhanced vestibulo-ocular response in an infant with esotropia should suggest the possibility of nystagmus compensation syndrome. I have found this observation especially helpful in young infants in whom careful observation during testing of ductions and versions is not always possible. 21
14
22
22
REFERENCES 1. Yee, R. D., Baloh, R. W., and Honrubia, V.: Study of congenital nystagmus. Optokinetic nystagmus. Br. J. Ophthalmol. 64:926, 1980. 2. von Noorden, G. K.: The nystagmus compensation (blockage) syndrome. Am. J . Ophthalmol. 82:283, 1976. 3. Ornitz, E . M., Atwell, C. W., Walter, D. O., Hartmann, E . E . , and Kaplan, A. R.: The maturation of vestibular nystagmus in infancy and childhood. Acta Otolaryngol. 88:244, 1979. 4. Eviatar, L . , Eviatar, A., and Naray, I.: Maturation of neurovestibular responses in infants. Dev. Med. Child Neurol. 16:435, 1974. 5. Eviatar, L . , Miranda, S., Eviatar, A., Freeman, K , and Borkowski, M.: Development of nystagmus in response to vestibular stimulation in infants. Ann. Neurol. 5:508, 1979. 6. Rossi, L . , Pignataro, O., Nino, L . , Gaini, R.,
708
AMERICAN JOURNAL OF OPHTHALMOLOGY
Sambataro, G., and Oldini, C : Maturation of vestibular responses in infants. Dev. Med. Child Neurol. 16:435, 1974. 7. Ritvo, E. R., Ornitz, E . , Eviatar, A., Markham, C. H., Brown, M. B., and Mason, A.: Decreased postrotatory nystagmus in early infantile autism. Neurology 19:653, 1969. 8. Rapin, I.: Hypoactive labyrinthe and motor development. Clin. Pediatr. 13:922, 1974. 9. Kanter, R. M., Clark, D. L . , Allen, L. C , and Chase, M. F.: Effects of vestibular stimulation on nystagmus response and motor performance in the developmentally delayed infant. Phys. Ther. 56:414, 1976. 10. Steinberg, M., and Rendle-Short, J.: Vestibular dysfunction in young children with minor neurological impairment. Dev. Med. Child Neurol. 19:639, 1977. 11. Doden, W., and Adams, A. : Elektronystagmographische Ergebnisse der Prüfung des optischvestibulären Systems bei Schielenden. Ber. Dtsch. Ophthalmol. Ges. 60:316, 1957. 12. Salman, S. D., and von Noorden, G. K.: Induced vestibular nystagmus in strabismic patients. Ann. Otol. Rhinol. Laryngol. 79:352, 1970. 13. Réthy, I.: Development of the simultaneous fixation from the divergent anatomic eye-positioning of the neonate. J. Pediatr. Ophthalmol. 6:92, 1969. 14. Hoyt, C. S., Mousel, D. K., and Weber,
JUNE, 1982
A. A. : Transient supranuclear disturbances of gaze in healthy neonates. Am. J. Ophthalmol. 89:708, 1980. 15. Fox, F . , Aslin, R., Shea, S., and Denap, S.: Stereopsis in human infants. Science 207:323, 1980. 16. Burian, H. M., and von Noorden, G. K.: Binocular Vision and Ocular Motility. Theory and Management of Strabismus, 2nd ed. St. Louis, C. V. Mosby, 1979, p. 284. 17. Réthy, I., and Gal, Z.: Results and principles of a new method of optical correction of hypermetropia in cases of esotropia. Acta Ophthalmol. 46:757, 1968. 18. Metz, H. S., and Smith, G.: Abduction nystagmus. J . Pediatr. Ophthalmol. Strabismus 15:312, 1978. 19. Buckley, E . , and Seaber, J. H.: Dyskinetic strabismus as a sign of cerebral palsy. Am. J. Ophthalmol. 91:652, 1981. 20. Mitsui, Y., Tamura, O., Hirai, K., Akazawa, K., Ohga, M., and Masuda, K.: An electromyographic study of esotropia. Br. ]. Ophthalmol. 65:161, 1981. 21. Trimble, J. L . , Ernest, J . T., and Newell, F. W. : Electro-oculography in infants. Invest. Ophthalmol. 16:669, 1977. 22. Schlossman, A., and Muchnick, R. S.: Nystagmus blockage. Classification and surgical management. In Reinecke, R. D. (ed.): Strabismus. New York, Grune and Stratton, 1979, p. 215.
M.D.
San Francisco, California
In 32 infants with congenital esotropia, I measured the vestíbuloocular response. The eight patients with nystagmus compensation syndrome exhibited brisk responses. Fourteen of the 24 who had esotropia without nystagmus had severely diminished responses and the other ten had moderate responses. Vestíbulo-ocular testing is useful in detecting subtle forms of nystagmus compensation syndrome, especially in young infants, in whom thorough examination of auctions and versions is difficult. Dysfunction of the vestibular system is not necessarily a primary cause of congenital esotropia, but brain-stem function in patients with congenital esotropia should be studied further.
When a full-term neonate is held at arms' length under the axillae, with his head tilted forward 30 degrees, and is rotated, his eyes deviate in the direction toward which the examiner is rotating the eye realignment, away from the direction of rotation. This vestibulo-ocular response induced by head movement produces a slow eye movement opposed to the infant's head movement, which decreases movement of the images on the retina. The slow components of the vestibulo-ocular response and optokinetic movement take place in the same direction and act synergistically to match the velocity of the head movement and more effectively stabilize the retinal images, thus improving vision. I found a consistent abnormality of the vestibulo-ocular response in infants with congenital esotropia that easily distin1
Accepted for publication Feb. 24, 1982. From the Departments of Ophthalmology and Pediatrics, University of California Medical Center, San Francisco, California. Reprint requests to Creig S. Hoyt, M.D., Room A-751, University of California, San Francisco, CA 94143. 704
guishes these children from those with nystagmus compensation syndrome. 2
SUBJECTS AND METHODS
I studied the vestibulo-ocular responses in 32 consecutive infants referred here with the diagnosis of congenital esotropia from February 1980 to October 1981. All of these patients had (1) onset of esotropia before the age of 6 months, documented by at least one examining ophthalmologist, (2) nonaccommodative esotropia present at all times and relatively stable in size of deviation, and (3) no known ocular or central nervous system disease other than abduction nystagmus. I considered children with esotropia and abduction nystagmus to have nystagmus compensation syndrome if they met the criteria outlined by von Noorden : (1) onset of esotropia in early infancy, (2) pseudoparesis of both abducens nerves, (3) head turn toward the side of the fixing eye, (4) absence of nystagmus with the fixing eye in adduction, and (5) appearance of a manifest jerk nystagmus as the fixing eye moved into primary position 2
© AMERICAN JOURNAL OF OPHTHALMOLOGY 93:704-708, 1982
VOL. 93, NO. 6
VESTIBULO-OCULAR RESPONSE IN ESOTROPIA
705
and abduction. Eight of the 32 infants vestibular stimulation, especially in the met these criteria. abducting eye. The other ten had a reI tested all the infants by standard sponse of 1 + in the fast phase. None of techniques of measuring the angle of stra- the patients with nystagmus compensabismus with the prism and cover test on tion syndrome exhibited a depressed ocuan accommodative target at 33 cm and on lar response to vestibular stimulation, a fixation light at 6 m. I analyzed the and none of the patients with congenital ductions and versions using various mov- esotropia demonstrated a brisk ocular reing fixation targets. I completed a cyclo- sponse. plegic refraction after instilling 1% atroDISCUSSION pine in both eyes of the infants on three consecutive days. The vestibular system is unique among Vestibular stimulation of the infants oculomotor subsystems because of its was provided by rotation. I held the rapid maturation in neonates. The vestibinfants vertically and facing me, with my ular system is anatomically complete and hands surrounding the infant's trunk. The functionally responsive at or before infant's head was bent forward 30 degrees birth. Newborn, full-term infants reover the body. Rotation of the infant 360 spond to acceleration. Their eyes deviate degrees around the examiner's axis pro- in the expected direction of the slow duced deviation of the eyes and head component, although acquisition of the opposite to the direction of rotation. A fast component with its probable pontine fast, recorrection ocular movement in the origin may be delayed in premature indirection of rotation represented the fants or those who are small for their other phase of the induced vestibulo- gestational age. " Children who have sufocular response. I graded this fast phase fered perinatal insults to the central nervas follows: 0 if no more than two to three ous system frequently fail to acquire this beats were seen with a single 360-degree fast component. rotation, 1 + if four to ten beats occurred, Vestibular dysfunction including alteraand 2 + if more than ten beats resulted tions in the vestibular ocular response from a single rotation. Normal, nonstra- reportedly occurs frequently in children bismic children usually exhibit a 2 + re- with various disorders involving minor sponse after the age of 1 month. I graded neurologic impairment. ' Abnormal ocuthe vestibulo-ocular response during ro- lar responses to vestibular stimulation tation, not upon completion of rotation. I have been reported in patients with strarotated the infants both clockwise and bismus. Doden and Adams described counterclockwise, paying special atten- involuntary, rhythmic, conjugate, pendution to the response of the abducting eye. lar deviations on vestibular testing of 23% of 150 patients with various forms of RESULTS strabismus. Salman and von Noorden The vestibulo-ocular responses of the reported a number of abnormal responses 32 infants are summarized in Tables 1 and to caloric stimulation in strabismic chil2. All eight patients with nystagmus com- dren, including postcaloric nystagmus of pensation syndrome demonstrated a irregular amplitude and frequency, vesbrisk ocular response to rotation. Four- tibular hyperexcitability, and irregular teen of the 24 patients with congenital eye movements with the eyes closed at esotropia without nystagmus demon- rest. Their report made no specific menstrated little or no fast ocular phase to tion of any abnormality of the vestibular 3
4
6
7 10
11,12
11
12
706
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1982
TABLE 1 CLINICAL FINDINGS IN C H I L D R E N W I T H CONGENITAL ESOTROPIA
Patient No., Sex, Age at First Examination (mos) 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24,
M, M, F, M, F, F, F, M, M, M, F, M, M, F, F, M, F, M, M, M, F, F, M, F,
3 7 11 6 16 4 9 8 4 2 6 5 5 2 8 29 4 5 3 6 8 5 11 4
Near
Distance
Fast Phase of Vestibulo-ocular Response*
55 60 45 70 60 50 60 60 60 55 40 65 60 55 70 65 50 30 65 45 60 70 55 70
55 60 45 70 60 50 60 60 50 55 40 65 60 55 60 65 50 30 65 45 60 70 57 70
0 1+ 0 1+ 0 0 1+ 1+ 0 1+ 1+ 0 0 0 1+ 1+ 0 0 0 0 1+ 0 1+ 0
Initial Deviation (Prism Diopters)
* Grading system: 0 = 2 to 3 beats/360-degree rotation; 1+ = 4 to 10 beats; and 2 + = more than 10 beats.
response in infants with congenital esotropia. Although the term "congenital esotropia" is well established, it is misleading. Newborns rarely have a constant, large-
angle esotropia; indeed, their eyes either are exotropic or exhibit a skew deviation. Therefore, neonatal esotropia might more correctly describe this earlyonset esotropia that presumably occurs 13
14
TABLE 2 CLINICAL FINDINGS IN C H I L D R E N W I T H NYSTAGMUS COMPENSATION SYNDROME
Patient No., Sex, Age at First Examination (mos) 1, 2, 3, 4, 5, 6, 7. 8,
M, M, F, M, F, M, F, M,
6 11 20 5 3 10 6 8
Near
Distance
Fast Phase of Vestibulo-ocular Response*
60 70 70 45 60 55 60 70
60 70 70 40 60 55 60 70
2+ 2+ 2+ 2+ 2+ 2+ 2+ 2+
Initial Deviation (Prism Diopters)
'Grading system: 0 = 2 to 3 beats/360-degree rotation; 1+ = 4 to 10 beats; and 2 + = more than 10 beats.
VOL.
93,
NO.
VESTIBULO-OCULAR RESPONSE IN ESOTROPIA
6
before the normal establishment of binocular reflexes. However, I use the term congenital rather than neonatal esotropia because it has been so well established. This condition is probably not the result of hyperopia or excessive accommodative effort, although the essentially nonaccommodative origin of congenital esotropia has been challenged. It is unlikely that injury to the abducens nerve is a primary cause of this disorder even in those patients with esotropia and abducting nystagmus. The specific factors that cause congenital esotropia remain to be defined, although a large number of affected patients show other overt signs of central nervous system dysfunction. Mitsui and colleagues' recent electromyographic study of patients with esotropia demonstrated that in some cases the medial recti muscles continued to fire tonically while the patient was under general anesthesia. When retrobulbar anesthesia was superimposed on one eye, the discharge from the ipsilateral medial rectus muscle decreased. However, this decrease was accompanied by a reciprocal increase in the discharge from the contralateral medial rectus muscle. Mitsui and associates suggested that this reciprocity could be explained by blockage of unilateral proprioception by the retrobulbar anesthesia. They did not know what factors might cause an abnormal excitation of proprioceptive impulses from extraocular muscles. However, their results suggest that the medial recti muscles are tonically driven by a neural system that is unaffected by general anesthesia. In light of this finding, it is not surprising that the duration of the fast phase of the vestibulo-ocular response, especially in the abducting eye, is attenuated in congenitally esotropic patients. Objective documentation of this abnormal vestibulo-ocular response is desirable, but it is difficult to record ocular move15
16
17
18
19
20
707
ment objectively in infants. The results of my study do not prove that congenital esotropia may be the result of damage to or miswiring of the vestibular ocular motor system. However, neonatal skew deviation may precede classic congenital esotropia, which supports vestibular dysfunction as a possible cause of congenital esotropia. Currently, vestibulo-ocular testing of congenitally esotropic patients is useful regardless of what it may indicate about the cause of this disorder. Overt cases of nystagmus compensation syndrome can be recognized easily, but subtle forms of the syndrome are easily overlooked. Moreover, the long-term prognosis for establishing a stable ocular alignment appears to be poorer in patients with nystagmus compensation syndrome than in those with esotropia without nystagmus. The recognition of subtle forms of the syndrome is, therefore, therapeutically and prognostically important. Finding an enhanced vestibulo-ocular response in an infant with esotropia should suggest the possibility of nystagmus compensation syndrome. I have found this observation especially helpful in young infants in whom careful observation during testing of ductions and versions is not always possible. 21
14
22
22
REFERENCES 1. Yee, R. D., Baloh, R. W., and Honrubia, V.: Study of congenital nystagmus. Optokinetic nystagmus. Br. J. Ophthalmol. 64:926, 1980. 2. von Noorden, G. K.: The nystagmus compensation (blockage) syndrome. Am. J . Ophthalmol. 82:283, 1976. 3. Ornitz, E . M., Atwell, C. W., Walter, D. O., Hartmann, E . E . , and Kaplan, A. R.: The maturation of vestibular nystagmus in infancy and childhood. Acta Otolaryngol. 88:244, 1979. 4. Eviatar, L . , Eviatar, A., and Naray, I.: Maturation of neurovestibular responses in infants. Dev. Med. Child Neurol. 16:435, 1974. 5. Eviatar, L . , Miranda, S., Eviatar, A., Freeman, K , and Borkowski, M.: Development of nystagmus in response to vestibular stimulation in infants. Ann. Neurol. 5:508, 1979. 6. Rossi, L . , Pignataro, O., Nino, L . , Gaini, R.,
708
AMERICAN JOURNAL OF OPHTHALMOLOGY
Sambataro, G., and Oldini, C : Maturation of vestibular responses in infants. Dev. Med. Child Neurol. 16:435, 1974. 7. Ritvo, E. R., Ornitz, E . , Eviatar, A., Markham, C. H., Brown, M. B., and Mason, A.: Decreased postrotatory nystagmus in early infantile autism. Neurology 19:653, 1969. 8. Rapin, I.: Hypoactive labyrinthe and motor development. Clin. Pediatr. 13:922, 1974. 9. Kanter, R. M., Clark, D. L . , Allen, L. C , and Chase, M. F.: Effects of vestibular stimulation on nystagmus response and motor performance in the developmentally delayed infant. Phys. Ther. 56:414, 1976. 10. Steinberg, M., and Rendle-Short, J.: Vestibular dysfunction in young children with minor neurological impairment. Dev. Med. Child Neurol. 19:639, 1977. 11. Doden, W., and Adams, A. : Elektronystagmographische Ergebnisse der Prüfung des optischvestibulären Systems bei Schielenden. Ber. Dtsch. Ophthalmol. Ges. 60:316, 1957. 12. Salman, S. D., and von Noorden, G. K.: Induced vestibular nystagmus in strabismic patients. Ann. Otol. Rhinol. Laryngol. 79:352, 1970. 13. Réthy, I.: Development of the simultaneous fixation from the divergent anatomic eye-positioning of the neonate. J. Pediatr. Ophthalmol. 6:92, 1969. 14. Hoyt, C. S., Mousel, D. K., and Weber,
JUNE, 1982
A. A. : Transient supranuclear disturbances of gaze in healthy neonates. Am. J. Ophthalmol. 89:708, 1980. 15. Fox, F . , Aslin, R., Shea, S., and Denap, S.: Stereopsis in human infants. Science 207:323, 1980. 16. Burian, H. M., and von Noorden, G. K.: Binocular Vision and Ocular Motility. Theory and Management of Strabismus, 2nd ed. St. Louis, C. V. Mosby, 1979, p. 284. 17. Réthy, I., and Gal, Z.: Results and principles of a new method of optical correction of hypermetropia in cases of esotropia. Acta Ophthalmol. 46:757, 1968. 18. Metz, H. S., and Smith, G.: Abduction nystagmus. J . Pediatr. Ophthalmol. Strabismus 15:312, 1978. 19. Buckley, E . , and Seaber, J. H.: Dyskinetic strabismus as a sign of cerebral palsy. Am. J. Ophthalmol. 91:652, 1981. 20. Mitsui, Y., Tamura, O., Hirai, K., Akazawa, K., Ohga, M., and Masuda, K.: An electromyographic study of esotropia. Br. ]. Ophthalmol. 65:161, 1981. 21. Trimble, J. L . , Ernest, J . T., and Newell, F. W. : Electro-oculography in infants. Invest. Ophthalmol. 16:669, 1977. 22. Schlossman, A., and Muchnick, R. S.: Nystagmus blockage. Classification and surgical management. In Reinecke, R. D. (ed.): Strabismus. New York, Grune and Stratton, 1979, p. 215.