Paradoxical eye movements have been described in various congenital and acquired ocular disorders, and different central and peripheral mechanisms have been proposed for its pathophysiology.1–3 Convergence movements on attempted side gaze have been reported in patients with horizontal gaze palsy. These paradoxical movements may be part of a near reflex substitution in which miosis and myopic shift in refraction accompany convergence movements.2 We describe a patient with right-sided facial colliculus syndrome due to pontine arteriovenus malformation, which manifested as near reflex substitution on attempting right gaze. We also report the results of this patient's strabismus surgery and provide a comprehensive review of the literature.
A 9-year-old girl was referred to the pediatric ophthalmology clinic for esotropia and abnormal head posture. Her medical history was remarkable for hydrocephalus secondary to intraventricular hemorrhage at age 1 month. Following this episode, she developed esotropia in her right eye. She was admitted to the neurosurgery service several times for recurring episodes of intraventricular hemorrhage and underwent insertion of an external ventricular drain. Cerebral angiography revealed a pontine arteriovenus malformation as the source of the intraventricular hemorrhage. The arteriovenus malformation was embolized when she was 6 years old. The intraventricular hemorrhage did not reoccur following the procedure, and her neurological and ocular signs and symptoms remained stable.
On ocular examination, her best corrected visual acuity was 20/60 and 20/20 in the right and left eyes, respectively. Her external examination was notable for a right face turn, right-sided facial weakness, lagophthalmos, and a mild paralytic lower eyelid ectropion. The motility examinations revealed a right esotropia of 35 prism diopters (PD). Attempting right gaze was associated with a convergence movement and subsequently increased esotropia and bilateral pupillary miosis. The amount of esotropia in the right gaze varied between 50 and 80 PD, depending on the patient's efforts to turn her eyes to the right (Figure 1).
(Top row) Facial weakness and lagophthalmos. (Middle row) Preoperative gaze position and convergence movement on attempted right gaze, showing (A) preoperative right face turn. (Bottom row) Postoperative gaze position and reduced convergence movement on attempted right gaze, showing (B) improved face turn to the right side postoperatively.
The oculocephalic maneuver could not elicit abduction in the right eye. The vertical eye movements were full. Refraction during the attempted right gaze revealed variable amounts of myopia (−3.00 to −8.00 diopters) in both eyes.
Magnetic resonance imaging of her brain revealed hypoplastic right sixth and seventh cranial nerves. The right lateral rectus muscle was atrophic. The arteriovenus malformation was evident at the facial colliculus and seemed large enough to involve the paramedian pontine reticular formation in addition to the right sixth nerve nucleus and facial nerve fascicle (Figure 2).
(A) (Axial) Fast imaging employing steady-state acquisition magnetic resonance imaging showing hypoplasia of abducens and facial nerves in pre-pontine cisternal space on the right side (white arrow) and normal abducens and facial nerves on the left side (black arrow). (B) (Orbital) Axial T1-weighted magnetic resonance imaging with contrast shows right lateral rectus atrophy.
We performed a right medial rectus muscle recession and a half-tendon transposition of the superior and inferior recti muscles to the right lateral rectus muscle insertion followed by a small lateral tarsorrhaphy. After the surgery, orthophoria was achieved in the primary position and the right face turn improved (Figure 1). The convergence movement on attempting right gaze was substantially decreased (Figure 1), but the miosis and myopic shift remained unchanged. Six months after the surgery, the ocular alignment and movements remained stable.
Simultaneous adduction movement of both eyes on attempting horizontal gaze in the presence of horizontal gaze palsy has been described in the literature using different terms. The term “convergence substitution” has been used if the abnormal adduction movement was accompanied by miosis or induced myopia. The term “synergistic convergence” has been used in the absence of miosis or induced myopia.1,2
The mechanism of this rare ocular movement disorder is not clearly understood. A peripheral (infranuclear) mechanism has been proposed for convergence movement without miosis or induced myopia, because it was reported in association with congenital fibrosis of the extraocular muscle.3 However, a similar abnormality has been described in brainstem dysplasia in a patient with horizontal gaze palsy with progressive scoliosis that cannot be explained by the peripheral mechanism.1,4
A central (supranuclear) mechanism has been proposed in the presence of miosis or induced myopia along with the convergence movement on attempted horizontal gaze.2,5
We suggest classifying the paradoxical adduction movements on attempted horizontal gaze in the following three categories.
Synergistic Adduction. In patients lacking miosis and induced myopia with either acquired peripheral insult6 or congenital cranial disinnervation disorder,3 the convergence system is not expected to be involved. Therefore, the term “synergistic adduction” seems more proper than “synergistic convergence.” Misdirection of the regenerative nerves (infranuclear) is a well-described mechanism for this phenomenon, as reported by Buckley et al.6 in the setting of orbital trauma.
Synergistic Convergence. This term may describe patients with horizontal gaze palsy secondary to a central lesion when the pupillary miosis and induced myopia do not accompany the convergence movement.4 Synergistic convergence has been reported in patients with horizontal gaze palsy and progressive scoliosis with ROBO3 mutation. In these patients, neuroimaging shows brainstem hypoplasia typical of horizontal gaze palsy with progressive scoliosis with intact cranial nerves 3 and 64; thus the regenerative misdirection of the ocular motor nerve is not the case in this syndrome. Khan et al.4 proposed that convergence movement without miosis and induced myopia might suggest different neuroanatomical localization for different components of the near reflex.
Near Reflex Substitution. This term may be applied if the pupillary miosis and induced myopia as two components of the near reflex accompany the convergence movement on attempted abduction as they do in the current study. Near reflex substitution has been previously reported in association with various central insults.5,7,8 Both synergistic convergence and near reflex (convergence) substitutions have been reported in horizontal gaze palsy with progressive scoliosis.2,4,9
In the current study, the hypoplastic sixth nerve in the cisternal space and the atrophic lateral rectus muscle on the right side may indicate infranuclear insults. However, the presence of miosis and induced myopia in addition to convergence movement during right gaze and the relatively large arteriovenus malformation, which seems to involve the sixth nerve nucleus and the pontine reticular formation, would also suggest a contributing supranuclear mechanism.
The synchronized activity of the version and vergence systems on attempting lateral gaze to fixate a target nearer than the optical infinity was suggested by Leigh and Zee.10 They proposed that the lesions of the version system, which are located in the pons, would result in overactivity of the vergence system located in the midbrain.10
In our patient, convergence movement on attempted right gaze was relatively reduced after surgery but miosis and induced myopia continued to present. Hayashi8 proposed that generating a small amount of abduction in the affected eye may mask the substituted convergence. This may explain the improvement of the synergistic convergence movement in our patient after the transposition procedure.
Kohono et al.5 reported postoperative under-correction of esotropia in a similar patient who had a medial rectus muscle recession and Jensen union procedure. They did not report whether the near reflex substitution changed after the surgery.
Near reflex substitution for the horizontal gaze palsy is a synergistic and involuntary ocular motility phenomenon induced by the voluntary attempt to abduct the affected eye. This phenomenon in a patient with other features of facial colliculus syndrome has been rarely reported. Eye muscle surgery reduced the paradoxical convergence movement but did not significantly improve the other components of the substituted near reflex.
- Bakbak B, Kansu T. Synergistic convergence and substituted convergence. Indian J Ophthalmol. 2013;61(2):82. doi:10.4103/0301-4738.107204 [CrossRef]
- Bakbak B, Kansu T. Acquired convergence substitution in horizontal gaze palsy and progressive scoliosis associated with ROBO3 mutations. Neuroophthalmology. 2012;36(5):203–207. doi:10.3109/01658107.2012.710920 [CrossRef]
- Kim JH, Hwang J-M. Adduction on attempted abduction: the opposite of synergistic divergence. Arch Ophthalmol. 2006;124(6):918–920. doi:10.1001/archopht.124.6.918 [CrossRef]
- Khan AO, Oystreck DT, Al-Tassan N, Al-Sharif L, Bosley TM. Bilateral synergistic convergence associated with homozygous ROB03 mutation (p.Pro771Leu). Ophthalmology. 2008;115(12):2262–2265. doi:10.1016/j.ophtha.2008.08.010 [CrossRef]
- Kohno T, Oohira A, Hori S. Near reflex substituting for acquired horizontal gaze palsy: a case report. Jpn J Ophthalmol. 2004;48(6):584–586. doi:10.1007/s10384-004-0113-8 [CrossRef]
- Buckley EG, Ellis FD, Postel E, Saunders T. Posttraumatic abducens to oculomotor nerve misdirection. J AAPOS. 2005;9(1):12–16. doi:10.1016/j.jaapos.2004.11.011 [CrossRef]
- Beigi B, O'Keeffe M, Logan P, Eustace P. Convergence substitution for paralysed horizontal gaze. Br J Ophthalmol. 1995;79(3):229–232. doi:10.1136/bjo.79.3.229 [CrossRef]
- Hayashi R. Convergence substitution in pontine tegmental hemorrhage: an observation with Frenzel goggles. Intern Med. 2006;45(8):553–555. doi:10.2169/internalmedicine.45.1652 [CrossRef]
- Bosley TM, Salih MA, Jen JC, et al. Neurologic features of horizontal gaze palsy and progressive scoliosis with mutations in ROBO3. Neurology. 2005;64(7):1196–1203. doi:10.1212/01.WNL.0000156349.01765.2B [CrossRef]
- Leigh RJ, Zee DS. The Neurology of Eye Movements, 3rd ed. New York: Oxford University Press; 1999.