Journal of the Neurological Sciences 353 (2015) 158–160
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Short communication
Gaze palsy and exotropia in internuclear ophthalmoplegia Ken Johkura a,b,⁎, Yosuke Kudo a,b, Yu Amano b, Hideyuki Kikyo b, Ryoko Imazeki b, Kazumitsu Amari c, Masahiro Yamamoto b a b c
Department of Neurology and Stroke Center, Hiratsuka Kyosai Hospital, Hiratsuka, Japan Department of Neurology, Yokohama Brain and Spine Center, Yokohama, Japan Department of Neuroendovascular Therapy, Yokohama Brain and Spine Center, Yokohama, Japan
a r t i c l e
i n f o
Article history: Received 19 February 2015 Received in revised form 19 March 2015 Accepted 9 April 2015 Available online 17 April 2015 Keywords: Internuclear ophthalmoplegia One-and-a-half syndrome Paralytic pontine exotropia Non-paralytic pontine exotropia
a b s t r a c t Background and purpose: Unilateral gaze palsy associated with internuclear ophthalmoplegia (INO), i.e., one-anda-half syndrome, is well known. Exotropia can also be associated with INO, but it has been reported only rarely. We sought to determine the frequencies and courses of gaze palsy and exotropia in INO. Methods: Patients hospitalized with acute-onset INO during the period January 2009 through December 2013 were identified from our clinical registry. Associated gaze palsy and exotropia were evaluated in the identified patients. Results: Twenty-five patients with unilateral INO and 7 patients with bilateral INO were included in this study. Of the 25 patients with unilateral INO, 4 (16.0.0%) had ipsilateral gaze palsy (one-and-a-half syndrome), 8 (32.0%) had exotropia (non-paralytic pontine exotropia), and 6 (24.0%) had both ipsilateral gaze palsy and exotropia (paralytic pontine exotropia). Six (85.7%) of the 7 patients with bilateral INO had exotropia. The gaze palsy persisted more than 1 week in 40.0% of patients, whereas the exotropia disappeared within 1 week in 92.9% of patients when the INO was unilateral. Conclusion: Exotropia is not uncommon in the acute stage of INO. However, it is often overlooked because of its short duration. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Internuclear ophthalmoplegia (INO) is an eye movement disorder characterized by adduction impairment due to a lesion involving the medial longitudinal fasciculus (MLF) [1]. Infarction and multiple sclerosis are the two leading causes [2,3], with multiple sclerosis being the most common cause in young patients and in patients with bilateral INO [4]. INO is sometimes accompanied by ipsilateral horizontal gaze palsy. The combination of INO and gaze palsy, called one-and-a-half syndrome [5], is well known. The mechanism of gaze palsy in one-and-a-half syndrome is simultaneous involvement of the paramedian pontine reticular formation (PPRF) or the abducens nucleus [6]. Exotropia can also occur with INO. Contralateral exotropia in INO is known as non-paralytic pontine exotropia [7], and exotropia in oneand-a-half syndrome is known as paralytic pontine exotropia [8]. However, exotropia associated with INO does not receive as much attention as gaze palsy. According to our previous observations, such exotropia
⁎ Corresponding author at: Department of Neurology, Yokohama Brain and Spine Center, 1-2-1 Takigashira, Isogo-ku, Yokohama 235-0012, Japan. Tel.: +81 45 753 2500; fax: +81 45 753 2879. E-mail address: [email protected] (K. Johkura).
http://dx.doi.org/10.1016/j.jns.2015.04.017 0022-510X/© 2015 Elsevier B.V. All rights reserved.
can be transient [9]; it might be due to over-excitation of the contralateral PPRF during fixation with the paretic eye [9,10]. In the retrospective study described herein, we sought to determine the actual frequencies of gaze palsy and exotropia in the acute stage of INO and to know the short-term courses of these two eye signs. 2. Methods We accessed the Hiratsuka Kyosai Hospital Stroke Registry to identify patients admitted for acute-onset INO between January 2009 and December 2013. Patients with chronic INO were excluded. Patients with another major neurological sign, such as hemiparesis, were also excluded. The causes of the INO had been determined on the basis of clinical criteria and course, laboratory tests, and radiologic studies, and photographic recordings of patients' eye movements were available to us. We calculated the incidences of associated gaze palsy and exotropia upon admission and examined the 1-week courses of both eye signs in the identified INO patients. The study was approved by our institutional ethics committee. 3. Results Thirty-two patients with INO were identified. The INO was unilateral in 25 patients (78.1%) and bilateral in 7 patients (21.9%). The causes of
K. Johkura et al. / Journal of the Neurological Sciences 353 (2015) 158–160
INO were infarction in 29 patients (90.6%), multiple sclerosis in 2 (6.3%), and hemorrhage in 1 (3.1%) (Table 1). In all 32 patients, lesions were located in the paramedian pontine tegmentum. Of the 25 patients with unilateral INO, 4 (16.0%) had ipsilateral gaze palsy (one-and-a-half syndrome), 8 (32.0%) had exotropia (non-paralytic pontine exotropia), and 6 (24.0%) had both ipsilateral gaze palsy and exotropia (paralytic pontine exotropia) (Table 1). The gaze palsies were uniformly ipsilateral. The exotropia was seen in the contralateral eye except in 1 patient (patient 15); ipsilateral eye exotropia was seen in this patient. One week after admission, although the exotropia had disappeared in 13 (92.9%) of the total 14 patients with exotropia, the gaze palsy had persisted in 4 (40.0%) of the total 10 patients with gaze palsy. In patients with gaze palsy and/or exotropia upon presentation, INO did not fully resolve during the first week. Of the 7 patients with bilateral INO, 6 (85.7%) had exotropia—either alternating exotropia (n = 5) or unilateral exotropia (n = 1) (Table 1). The exotropia disappeared in only 2 (33.3%) of these 6 patients during the first week after admission. The bilateral INO persisted beyond the first week in all 7 patients. 4. Discussion In most of our patients, the cause of the INO was infarction. In Western countries, multiple sclerosis is also reported to be a very common cause of INO, especially when the INO is bilateral [2–4]. However, in our series, the INO was due to multiple sclerosis in only 2 patients, and bilateral INO was caused by infarction in 6 of 7 patients. This difference in cause may be due to the paucity of multiple sclerosis in Asia [11]. Unilateral INO was accompanied by ipsilateral gaze palsy upon admission in 10 (40.0%) of 25 patients; thus, these patients presented
159
with one-and-a-half syndrome. The previous reported incidences of gaze palsy associated with unilateral INO (one-and-a-half syndrome) are about half the incidence that we documented [3,11]. Because gaze palsy in INO tends to improve with time [11], the high incidence of gaze palsy among our patients might be explained by the timing of the examinations; i.e., it's possible that our patients were examined earlier than those reported previously. Unlike the well-documented association between INO and gaze palsy, exotropia in INO has only rarely been reported. However, in our patient series, exotropia was more frequently associated with INO than was gaze palsy; it was seen in 14 (56.0%) of the 25 patients with unilateral acute-stage INO. Exotropia in INO patients has usually been reported in the contralateral eye [9,10], and the exotropia was contralateral in most of our patients also. However, ipsilateral exotropia was seen in 1 of our patients. Ipsilateral exotropia has also been reported previously [12]. In almost all of our patients with unilateral INO, the exotropia disappeared within 1 week. To the contrary, the gaze palsy persisted beyond the first week after admission in half of our patients. The short duration of exotropia may explain the paucity of reports concerning INOassociated exotropia. Our findings indicate that exotropia is not an uncommon eye sign in the acute stage of INO. In our patients with bilateral INO, exotropia was also common, seen in 6 (85.7%) of the 7 patients, and the exotropia did not resolve in most cases of bilateral INO. Alternating exotropia with bilateral INO has well been documented [13], but this is probably because of its long duration. In conclusion, our study findings indicate that exotropia is common in the acute stage of INO. The common occurrence of exotropia seems to have been overlooked because it resolves within a short period.
Table 1 Study patients with internuclear ophthalmoplegia and their symptoms. Patient no./age/sex
Etiology
1/85/F 2/67/M 3/65/M 4/82/F 5/58/M 6/62/F 7/30/F 8/83/F 9/73/M 10/61/M 11/79/M 12/59/M 13/44/M 14/66/M 15/41/M 16/77/M 17/73/M 18/70/M 19/50/F 20/50/F 21/83/F 22/48/M 23/77/F 24/69/F 25/75/F 26/55/M 27/59/M 28/49/M 29/50/M 30/75/M 31/75/M 32/33/F
Infarct Infarct Infarct Infarct Infarct Hemorrhage MS Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct MS
Chief eye sign Rt INO Lt INO Lt INO Lt INO Rt INO Rt INO Lt INO Rt INO Rt INO Lt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Lt INO Lt INO Lt INO Rt INO Lt INO Lt INO Lt INO Bil INO Bil INO Bil INO Bil INO Bil INO Bil INO Bil INO
Associated eye sign(s) Upon admission
Lt exotropia Lt exotropia Rt exotropia Lt exotropia Lt exotropia Lt exotropia Lt exotropia Rt exotropia Rt gaze palsy Rt gaze palsy Rt gaze palsy Lt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Lt exotropia, Rt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Lt exotropia Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia
Note that age is shown in years. M = male, F = female, INO = internuclear ophthalmoplegia, Rt = right, Lt = left, Bil = bilateral, MS = multiple sclerosis.
1 week later
Rt gaze palsy
Lt gaze palsy Lt gaze palsy Lt gaze palsy Rt exotropia
Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia
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K. Johkura et al. / Journal of the Neurological Sciences 353 (2015) 158–160
Conflict of interest The authors have no conflicts of interest to disclose. References [1] Smith JL, Cogan DG. Internuclear ophthalmoplegia: a review of fifty-eight cases. Arch Ophthalmol 1959;61:687–94. [2] Keane JR. Internuclear ophthalmoplegia: unusual causes in 114 of 410 patients. Arch Neurol 2005;62:714–7. [3] Bolaños I, Lozano D, Cantú C. Internuclear ophthalmoplegia: causes and long-term follow-up in 65 patients. Acta Neurol Scand 2004;110:161–5. [4] Gonyea EF. Bilateral internuclear ophthalmoplegia: association with occlusive cerebrovascular disease. Arch Neurol 1974;31:168–73. [5] Fisher CM. Some neuro-ophthalmological observations. J Neurol Neurosurg Psychiatry 1967;30:383–92. [6] Wall M, Wray SH. The one-and-a-half syndrome—a unilateral disorder of the pontine tegmentum: a study of 20 cases and review of the literature. Neurology 1983;33: 971–80.
[7] Bogousslavsky J, Regli F. Paralytic and non-paralytic pontine exotropia. Rev Neurol 1983;139:219–23. [8] Sharpe JA, Rosenberg MA, Hoyt WF, Daroff RB. Paralytic pontine exotropia. A sign of acute unilateral pontine gaze palsy and internuclear ophthalmoplegia. Neurology 1974;24:1076–81. [9] Komiyama A, Takamatsu K, Johkura K, Hasegawa O, Fukutake T, Hiratama K. Internuclear ophthalmoplegia and contralateral exotropia: nonparalytic pontine exotropia and WEBINO syndrome. Neuroophthalmology 1998;19:33–44. [10] Johkura K, Komiyama A, Kuroiwa Y. Eye deviation in patients with one-and-a-half syndrome. Eur Neurol 2000;44:210–5. [11] Kim JS. Internuclear ophthalmoplegia as an isolated or predominant symptom of brainstem infarction. Neurology 2004;62:1491–6. [12] Ikeda Y, Okamoto K. Lesion responsible for WEMINO syndrome confirmed by magnetic resonance imaging. J Neurol Neurosurg Psychiatry 2002;73:204–5. [13] Hoyt WF, Daroff RB. Supranuclear disorders of ocular control systems in man. Clinical, anatomical, and physiological correlations—1969. In: Bachy-Rita P, Collins CC, Hyde JE, editors. The control of eye movement. New York: Academic Press; 1971. p. 175–235.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Short communication
Gaze palsy and exotropia in internuclear ophthalmoplegia Ken Johkura a,b,⁎, Yosuke Kudo a,b, Yu Amano b, Hideyuki Kikyo b, Ryoko Imazeki b, Kazumitsu Amari c, Masahiro Yamamoto b a b c
Department of Neurology and Stroke Center, Hiratsuka Kyosai Hospital, Hiratsuka, Japan Department of Neurology, Yokohama Brain and Spine Center, Yokohama, Japan Department of Neuroendovascular Therapy, Yokohama Brain and Spine Center, Yokohama, Japan
a r t i c l e
i n f o
Article history: Received 19 February 2015 Received in revised form 19 March 2015 Accepted 9 April 2015 Available online 17 April 2015 Keywords: Internuclear ophthalmoplegia One-and-a-half syndrome Paralytic pontine exotropia Non-paralytic pontine exotropia
a b s t r a c t Background and purpose: Unilateral gaze palsy associated with internuclear ophthalmoplegia (INO), i.e., one-anda-half syndrome, is well known. Exotropia can also be associated with INO, but it has been reported only rarely. We sought to determine the frequencies and courses of gaze palsy and exotropia in INO. Methods: Patients hospitalized with acute-onset INO during the period January 2009 through December 2013 were identified from our clinical registry. Associated gaze palsy and exotropia were evaluated in the identified patients. Results: Twenty-five patients with unilateral INO and 7 patients with bilateral INO were included in this study. Of the 25 patients with unilateral INO, 4 (16.0.0%) had ipsilateral gaze palsy (one-and-a-half syndrome), 8 (32.0%) had exotropia (non-paralytic pontine exotropia), and 6 (24.0%) had both ipsilateral gaze palsy and exotropia (paralytic pontine exotropia). Six (85.7%) of the 7 patients with bilateral INO had exotropia. The gaze palsy persisted more than 1 week in 40.0% of patients, whereas the exotropia disappeared within 1 week in 92.9% of patients when the INO was unilateral. Conclusion: Exotropia is not uncommon in the acute stage of INO. However, it is often overlooked because of its short duration. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Internuclear ophthalmoplegia (INO) is an eye movement disorder characterized by adduction impairment due to a lesion involving the medial longitudinal fasciculus (MLF) [1]. Infarction and multiple sclerosis are the two leading causes [2,3], with multiple sclerosis being the most common cause in young patients and in patients with bilateral INO [4]. INO is sometimes accompanied by ipsilateral horizontal gaze palsy. The combination of INO and gaze palsy, called one-and-a-half syndrome [5], is well known. The mechanism of gaze palsy in one-and-a-half syndrome is simultaneous involvement of the paramedian pontine reticular formation (PPRF) or the abducens nucleus [6]. Exotropia can also occur with INO. Contralateral exotropia in INO is known as non-paralytic pontine exotropia [7], and exotropia in oneand-a-half syndrome is known as paralytic pontine exotropia [8]. However, exotropia associated with INO does not receive as much attention as gaze palsy. According to our previous observations, such exotropia
⁎ Corresponding author at: Department of Neurology, Yokohama Brain and Spine Center, 1-2-1 Takigashira, Isogo-ku, Yokohama 235-0012, Japan. Tel.: +81 45 753 2500; fax: +81 45 753 2879. E-mail address: [email protected] (K. Johkura).
http://dx.doi.org/10.1016/j.jns.2015.04.017 0022-510X/© 2015 Elsevier B.V. All rights reserved.
can be transient [9]; it might be due to over-excitation of the contralateral PPRF during fixation with the paretic eye [9,10]. In the retrospective study described herein, we sought to determine the actual frequencies of gaze palsy and exotropia in the acute stage of INO and to know the short-term courses of these two eye signs. 2. Methods We accessed the Hiratsuka Kyosai Hospital Stroke Registry to identify patients admitted for acute-onset INO between January 2009 and December 2013. Patients with chronic INO were excluded. Patients with another major neurological sign, such as hemiparesis, were also excluded. The causes of the INO had been determined on the basis of clinical criteria and course, laboratory tests, and radiologic studies, and photographic recordings of patients' eye movements were available to us. We calculated the incidences of associated gaze palsy and exotropia upon admission and examined the 1-week courses of both eye signs in the identified INO patients. The study was approved by our institutional ethics committee. 3. Results Thirty-two patients with INO were identified. The INO was unilateral in 25 patients (78.1%) and bilateral in 7 patients (21.9%). The causes of
K. Johkura et al. / Journal of the Neurological Sciences 353 (2015) 158–160
INO were infarction in 29 patients (90.6%), multiple sclerosis in 2 (6.3%), and hemorrhage in 1 (3.1%) (Table 1). In all 32 patients, lesions were located in the paramedian pontine tegmentum. Of the 25 patients with unilateral INO, 4 (16.0%) had ipsilateral gaze palsy (one-and-a-half syndrome), 8 (32.0%) had exotropia (non-paralytic pontine exotropia), and 6 (24.0%) had both ipsilateral gaze palsy and exotropia (paralytic pontine exotropia) (Table 1). The gaze palsies were uniformly ipsilateral. The exotropia was seen in the contralateral eye except in 1 patient (patient 15); ipsilateral eye exotropia was seen in this patient. One week after admission, although the exotropia had disappeared in 13 (92.9%) of the total 14 patients with exotropia, the gaze palsy had persisted in 4 (40.0%) of the total 10 patients with gaze palsy. In patients with gaze palsy and/or exotropia upon presentation, INO did not fully resolve during the first week. Of the 7 patients with bilateral INO, 6 (85.7%) had exotropia—either alternating exotropia (n = 5) or unilateral exotropia (n = 1) (Table 1). The exotropia disappeared in only 2 (33.3%) of these 6 patients during the first week after admission. The bilateral INO persisted beyond the first week in all 7 patients. 4. Discussion In most of our patients, the cause of the INO was infarction. In Western countries, multiple sclerosis is also reported to be a very common cause of INO, especially when the INO is bilateral [2–4]. However, in our series, the INO was due to multiple sclerosis in only 2 patients, and bilateral INO was caused by infarction in 6 of 7 patients. This difference in cause may be due to the paucity of multiple sclerosis in Asia [11]. Unilateral INO was accompanied by ipsilateral gaze palsy upon admission in 10 (40.0%) of 25 patients; thus, these patients presented
159
with one-and-a-half syndrome. The previous reported incidences of gaze palsy associated with unilateral INO (one-and-a-half syndrome) are about half the incidence that we documented [3,11]. Because gaze palsy in INO tends to improve with time [11], the high incidence of gaze palsy among our patients might be explained by the timing of the examinations; i.e., it's possible that our patients were examined earlier than those reported previously. Unlike the well-documented association between INO and gaze palsy, exotropia in INO has only rarely been reported. However, in our patient series, exotropia was more frequently associated with INO than was gaze palsy; it was seen in 14 (56.0%) of the 25 patients with unilateral acute-stage INO. Exotropia in INO patients has usually been reported in the contralateral eye [9,10], and the exotropia was contralateral in most of our patients also. However, ipsilateral exotropia was seen in 1 of our patients. Ipsilateral exotropia has also been reported previously [12]. In almost all of our patients with unilateral INO, the exotropia disappeared within 1 week. To the contrary, the gaze palsy persisted beyond the first week after admission in half of our patients. The short duration of exotropia may explain the paucity of reports concerning INOassociated exotropia. Our findings indicate that exotropia is not an uncommon eye sign in the acute stage of INO. In our patients with bilateral INO, exotropia was also common, seen in 6 (85.7%) of the 7 patients, and the exotropia did not resolve in most cases of bilateral INO. Alternating exotropia with bilateral INO has well been documented [13], but this is probably because of its long duration. In conclusion, our study findings indicate that exotropia is common in the acute stage of INO. The common occurrence of exotropia seems to have been overlooked because it resolves within a short period.
Table 1 Study patients with internuclear ophthalmoplegia and their symptoms. Patient no./age/sex
Etiology
1/85/F 2/67/M 3/65/M 4/82/F 5/58/M 6/62/F 7/30/F 8/83/F 9/73/M 10/61/M 11/79/M 12/59/M 13/44/M 14/66/M 15/41/M 16/77/M 17/73/M 18/70/M 19/50/F 20/50/F 21/83/F 22/48/M 23/77/F 24/69/F 25/75/F 26/55/M 27/59/M 28/49/M 29/50/M 30/75/M 31/75/M 32/33/F
Infarct Infarct Infarct Infarct Infarct Hemorrhage MS Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct Infarct MS
Chief eye sign Rt INO Lt INO Lt INO Lt INO Rt INO Rt INO Lt INO Rt INO Rt INO Lt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Rt INO Lt INO Lt INO Lt INO Rt INO Lt INO Lt INO Lt INO Bil INO Bil INO Bil INO Bil INO Bil INO Bil INO Bil INO
Associated eye sign(s) Upon admission
Lt exotropia Lt exotropia Rt exotropia Lt exotropia Lt exotropia Lt exotropia Lt exotropia Rt exotropia Rt gaze palsy Rt gaze palsy Rt gaze palsy Lt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Lt exotropia, Rt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Rt exotropia, Lt gaze palsy Lt exotropia Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia
Note that age is shown in years. M = male, F = female, INO = internuclear ophthalmoplegia, Rt = right, Lt = left, Bil = bilateral, MS = multiple sclerosis.
1 week later
Rt gaze palsy
Lt gaze palsy Lt gaze palsy Lt gaze palsy Rt exotropia
Alternating exotropia Alternating exotropia Alternating exotropia Alternating exotropia
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K. Johkura et al. / Journal of the Neurological Sciences 353 (2015) 158–160
Conflict of interest The authors have no conflicts of interest to disclose. References [1] Smith JL, Cogan DG. Internuclear ophthalmoplegia: a review of fifty-eight cases. Arch Ophthalmol 1959;61:687–94. [2] Keane JR. Internuclear ophthalmoplegia: unusual causes in 114 of 410 patients. Arch Neurol 2005;62:714–7. [3] Bolaños I, Lozano D, Cantú C. Internuclear ophthalmoplegia: causes and long-term follow-up in 65 patients. Acta Neurol Scand 2004;110:161–5. [4] Gonyea EF. Bilateral internuclear ophthalmoplegia: association with occlusive cerebrovascular disease. Arch Neurol 1974;31:168–73. [5] Fisher CM. Some neuro-ophthalmological observations. J Neurol Neurosurg Psychiatry 1967;30:383–92. [6] Wall M, Wray SH. The one-and-a-half syndrome—a unilateral disorder of the pontine tegmentum: a study of 20 cases and review of the literature. Neurology 1983;33: 971–80.
[7] Bogousslavsky J, Regli F. Paralytic and non-paralytic pontine exotropia. Rev Neurol 1983;139:219–23. [8] Sharpe JA, Rosenberg MA, Hoyt WF, Daroff RB. Paralytic pontine exotropia. A sign of acute unilateral pontine gaze palsy and internuclear ophthalmoplegia. Neurology 1974;24:1076–81. [9] Komiyama A, Takamatsu K, Johkura K, Hasegawa O, Fukutake T, Hiratama K. Internuclear ophthalmoplegia and contralateral exotropia: nonparalytic pontine exotropia and WEBINO syndrome. Neuroophthalmology 1998;19:33–44. [10] Johkura K, Komiyama A, Kuroiwa Y. Eye deviation in patients with one-and-a-half syndrome. Eur Neurol 2000;44:210–5. [11] Kim JS. Internuclear ophthalmoplegia as an isolated or predominant symptom of brainstem infarction. Neurology 2004;62:1491–6. [12] Ikeda Y, Okamoto K. Lesion responsible for WEMINO syndrome confirmed by magnetic resonance imaging. J Neurol Neurosurg Psychiatry 2002;73:204–5. [13] Hoyt WF, Daroff RB. Supranuclear disorders of ocular control systems in man. Clinical, anatomical, and physiological correlations—1969. In: Bachy-Rita P, Collins CC, Hyde JE, editors. The control of eye movement. New York: Academic Press; 1971. p. 175–235.
