Electrophysiology of Extraocular Cranial Nerves: Oculomotor, Trochlear, and Abducens Nerve.

The utility of extraocular cranial nerve electrophysiologic recordings lies primarily in the operating room during skull base surgeries. Surgical manipulation during skull base surgeries poses a risk of injury to multiple cranial nerves, including those innervating extraocular muscles. Because tumors distort normal anatomic relationships, it becomes particularly challenging to identify cranial nerve structures. Studies have reported the benefits of using intraoperative spontaneous electromyographic recordings and compound muscle action potentials evoked by electrical stimulation in preventing postoperative neurologic deficits. Apart from surgical applications, electromyography of extraocular muscles has also been used to guide botulinum toxin injections in patients with strabismus and as an adjuvant diagnostic test in myasthenia gravis. In this article, we briefly review the rationale, current available techniques to monitor extraocular cranial nerves, technical difficulties, clinical and surgical applications, as well as future directions for research.

Strabismus.

Defining the type of strabismus creates a framework for work-up and management. Comitant esotropia is most commonly a childhood condition treated with glasses and surgery. Comitant exotropia is often a childhood condition that may require surgical correction. Microvascular disease is the most common cause of ocular cranial nerve palsies in adult patients.

Skew deviation e ocular tilt reaction versus paralisia do nervo troclear / Skew deviation and ocular tilt reaction versus trochlear nerve palsy

Skew deviation é o desalinhamento vertical dos olhos causado por disfunção unilateral no tronco cerebral, cerebelo ou sistema vestibular periférico, comprometendo as vias por onde transitam impulsos dos órgãos otolíticos aos núcleos oculomotores. Está frequentemente associado a torção ocular e inclinação da cabeça, compondo, assim, a ocular tilt reaction. Neste artigo os autores ressaltam aspectos históricos, fisiológicos, etiopatogênicos e clínicos que contribuem para caracterizar ambas as condições, além da diferenciação clínica com a paralisia do nervo troclear.

Skew deviation is the vertical misalignment of the eyes caused by unilateral dysfunction in the brain stem, cerebellum or peripheral vestibular system, resulting imbalance in otolith input to the oculo-motor system. It's often associated with ocular torsion and head tilt, which together comprise the ocular tilt reaction. In this article the authors emphasize the historical, physiological, etiopathogenesis and clinical aspects that contribute to characterize both conditions, and help to differentiate them clinically from trochlear nerve palsy.

Infranuclear ocular motor disorders.

This chapter covers the very large number of possible disorders that can affect the three ocular motor nerves, the neuromuscular junction, or the extraocular muscles. Conditions affecting the nerves are discussed under two major headings: those in which the site of damage can be anatomically localized (e.g., fascicular lesions and lesions occurring in the subarachnoid space, the cavernous sinus, the superior orbital fissure, or the orbit) and those in which the site of the lesion is either nonspecific or variable (e.g., vascular lesions, tumors, "ophthalmoplegic migraine," and congenital disorders). Specific comments on the diagnosis and management of disorders of each of the three nerves follow. Ocular motor synkineses (including Duane's retraction syndrome and aberrant regeneration) and disorders resulting in paroxysms of excess activity (e.g., neuromyotonia) are then covered, followed by myasthenia gravis and other disorders that affect the neuromuscular junction. A final section discusses disorders of the extraocular muscles themselves, including thyroid disease, orbital myositis, mitochondrial disease, and the muscular dystrophies.

[Intraoperative identification of oculomotor, trochlear and abducent nerves in surgery of invasive cranioorbital tumors (new technique)].

BACKGROUND: Aim of the study was to evaluate effectiveness of intraoperative identification of oculomotor nerves (OMN) in resection of skull base tumors invading superior orbital fissure and cavernous sinus. MATERIALS AND METHODS: 69 patients with cranioorbital tumors operated in Burdenko Neurosurgical Institute (Moscow, Russia) since 2000 until 2005 were included in the study. They were divided into 2 groups: 19 patients treated with intraoperative identification of OMN and 50 patients in the control group. Craniorbital meningiomas were in the majority among all cases. Intraoperative identification of OMN was performed using coaxial electrode while muscular response was registered through electrodes inserted in m. levator palpebrae superioris, m. obliquus superior and m. rectus lateralis (for III, IV and VI cranial nerves, respectively). Identification of IMN trunci was repeated throughout the whole stage of tumor resection for their preservation. RESULTS: comparison of dynamics of oculomotor dysfunction in early postoperative period in patients of both groups demonstrated that intraoperative identification of OMN allowed to decrease the frequency of oculomotor deficit. The rates in main and control groups were: for III and IV nerves--37% and 68% (p < 0.05), for VI nerve--47% and 54% (p > 0.05), respectively. CONCLUSION: application of intraoperative identification of OMN allows to decrease the risk of oculomotor deterioration due to III and IV nerve dysfunction by 1.8 times. Technically the method is quite simple and not time-consuming procedure.

The effect of acute superior oblique palsy on vertical pursuit in monkeys.

PURPOSE: To investigate vertical smooth pursuit eye movements in monkeys with acute acquired superior oblique palsy (SOP). METHODS: The trochlear nerve was severed intracranially in two rhesus monkeys. After surgery, the paretic eye was patched for 6 or 9 days, and then binocular viewing was allowed. Eye movements were measured with binocular, dual search coils, before and after surgery, under monocular viewing conditions. Vertical pursuit movements along the midline were elicited by using triangular-wave (20 deg/s, +/-20 degrees ) or step-ramp (20 deg/s) stimuli at a distance of 66 cm. RESULTS: During the early post-lesion period, before binocular viewing was allowed, pursuit velocity of the paretic eye during triangular-wave tracking was lower than that of the normal eye. When the viewing eye crossed straight ahead, the changes in pursuit velocity conjugacy were similar for upward and downward tracking. After habitual binocular viewing was allowed, differences between upward and downward pursuit emerged. When measured approximately 30 days after lesioning, this directional asymmetry was less during the open-loop period of step-ramp tracking than during triangular-wave tracking. CONCLUSIONS: Rhesus monkeys with acute acquired SOP show characteristic changes in vertical pursuit, with deficits for both upward and downward tracking, and differences between the initiation of step-ramp pursuit and the sustained response during triangular-wave tracking. The habitual viewing condition (monocular versus binocular) also affected the pattern of deficit.

The role of intraoperative monitoring of oculomotor and trochlear nuclei -safe entry zone to tegmental lesions.

OBJECTIVE: A safe entry zone to tegmental lesions was identified based on intraoperative electrophysiological findings, the compound muscle action potentials (CMAP) from the extraocular muscles, and anatomic considerations. This entry zone is bordered caudally by the intramesencephalic path of the trochlear, laterally by the spinothalamic tract, and rostrally by the caudal margin of the brachium of the superior colliculus. METHODS: Four intrinsic midbrain lesions were operated upon via the safe entry zone using the infratentorial paramedian supracerebellar approach. All lesions involved the tegmentum and included an anaplastic astrocytoma, a metastatic brain tumor, a radiation necrosis, and a cavernous angioma. CMAP were bilaterally monitored from the inferior recti (for oculomotor function) and superior oblique (for trochlear nerve function) muscles. RESULTS: In three of four cases, CMAP related to the oculomotor nerve were obtained upon stimulation at the cavity wall after removal of the tumor. Stimulation at the surface of the quadrigeminal plate, however, did not cause any CMAP response. Using this monitoring as an indicator, the lesions were totally removed. CONCLUSIONS: In the surgery of tegmental lesions, CMAP monitoring from extraocular muscles is particularly helpful to prevent damage to crucial neural structures during removal of intrinsic lesions, but less so to select the site of the medullary incision. The approach via the lateral part of the colliculi is considered to be a safe route to approach the tegmental lesions.

Influencia vestibular en la respuesta a la maniobra de Bielschowsky en parálisis del cuarto nervio craneal / Vestibular influence in the response to Bielschowsky maneuver in fourth cranial nerve palsy

Objetivo: Describir en una serie de pacientes con parálisis unilateral del cuarto nervio craneal, la diferencia de la desviación vertical en posición erecta y supina. Material y método: Se incluyeron pacientes con diagnóstico de parálisis del cuarto nervio craneal unilateral, realizando exploración oftalmológica completa así como medición de la desviación con prismas y oclusión alterna en posición erecta y en posición supina realizando la maniobra de Bielschowsky. Resultados: Se exploraron 13 pacientes con el diagnóstico antes mencionado; la mayor parte de ellos presentaron menor desviación vertical en posición supina; así mismo al realizar la maniobra de Bielschowsky, la respuesta en posición supina fue menor que la presentada en posición erecta. Conclusiones: Los reflejos vestíbulo oculares, responsable de la mayor desviación vertical al inclinar la cabeza hacia el lado parético en casos de parálisis del nervio troclear, se atenúan en posición supina. La explicación fisiológica se basa en el control de los movimientos oculares por parte de los otolitos, los cuales reciben estimulación de a cuerdo a su posición en relación a la gravedad; esta observación clínica apoya la explicación propuesta por Bielschowsky sobre la participación del aparato vestibular en uno de los principales signos clínicos de esta entidad.

Purpose. To describe vertical deviation differences in a group of patients with unilateral fourth cranial nerve palsy in erect versus supine position. Methods. We included patients with unilateral fourth cranial nerve palsy who underwent full ophthalmologic exploration and measurement of the vertical deviation with prisms and alternate occlusion in erect and supine position performing Bielschowsky´s test. Results. Thirteen patients were explored; most of them showed less vertical deviation in the supine position, the response to the Bielschowsky´s test was smaller in the supine position than in the erect patient. Conclusion. The vestibulo-ocular reflexes responsible for the larger vertical deviation when tilting the head to the paretic side, are attenuated in the supine position; the physiologic explanation of this phenomenon is based on the otholits role in the control of ocular movements; these receptors are stimulated according to their position in relation to gravity. This clinical observation supports the explanation proposed by Bielschowsky about the role of the vestibular system in one of the main clinical sings of this entity.

Proposed treatment strategy for cavernous sinus meningiomas: a prospective study.

OBJECTIVE: To establish a safe and effective treatment strategy for cavernous sinus (CS) meningiomas, we prospectively analyzed the outcome of a treatment protocol combining surgery and radiosurgery during the past 7 years. METHODS: Tumors confined to the CS and distant from the optic apparatus and the brainstem were treated with radiosurgery alone. Tumors attached to or compressing the optic apparatus and brainstem and that were larger than 3 cm in mean diameter, extended into the multiple cranial fossae, and were suspected of being malignant were treated with combined nonradical microsurgery and radiosurgery. RESULTS: In accordance with this treatment protocol, 40 patients aged 26 to 72 years (median, 51 yr) with primary (n = 27) or recurrent (n = 13) CS meningiomas (volume range, 0.9-39.3 cm(3); median volume, 5.4 cm(3)) were treated with combined surgery and radiosurgery (n = 23) or radiosurgery alone (n = 17). During radiosurgery, 12 to 18 Gy (median, 16 Gy) was delivered to the tumor margin. The follow-up period ranged from 14 to 79 months (median, 47 mo). The actuarial tumor control rate was 94.1% at 5 years. The improvement of cranial nerve function was significantly frequent in patients with primary CS meningiomas (P < 0.05). Permanent cranial nerve dysfunction was significantly frequent in patients with tumors compressing the brainstem or smaller than 10 cm(3) (P < 0.05). All 36 patients with a pretreatment Karnofsky Performance Scale score of 90 or more maintained the same range after treatment. CONCLUSION: Proper combination of microsurgery and radiosurgery for CS meningiomas provides excellent growth control with favorable functional state. Outcomes were better when this protocol was adopted at the initial diagnosis for patients with smaller tumors that did not compress the brainstem.

Intra-Operative electromyographic monitoring of extra-ocular motor nerves (Nn. III, VI) in skull base surgery.

BACKGROUND: Extraocular motor nerves (Nn. III, IV, VI) are at risk of damage during skull base surgery. A new recording technique was employed in 18 patients suffering from various skull base tumours in order to extend intra-operative EMG monitoring to the extra-ocular muscles. METHODS: Selective intra-operative EMG recordings were obtained from extra-ocular muscles by placement of single-shafted bipolar needle electrodes under the guidance of B-mode ultrasound to visualise the needle tip within the target muscle in the orbital cavity. FINDINGS: Following bipolar electrical stimulation, the oculomotor nerve (N.III) was intra-operatively identified in 5 out of 7 cases, and the abducens nerve (N.VI) in 12 out of 18 cases. Postoperative (3-6 months) oculomotor nerve function remained unchanged in 5 and improved in 2 patients. No permanent deterioration was observed. Abducens nerve function deteriorated in two patients and improved in one case, but remained unchanged in 15 cases. No side effects occurred. There was neither any distinct relation of ocular motor nerve function to the kind and extent of SMA ("spontaneous muscle activity") patterns, nor could such relationship be detected with concern to neurophysiological parameters (latencies, amplitudes) of electrically evoked CMAP ("compound muscle action potentials"). INTERPRETATION: The EMG technique proposed proved to be mainly effective as a mapping tool for intra-operative localisation and identification of ocular motor nerves in skull base surgery. However, the predictive value of conventional neurophysiological parameters for clinical outcome, seems to be rather poor. Further studies on a larger number of patients are therefore required to develop new quantification techniques which enable an intra-operative prediction of ocular motor nerve deficits. Further efforts are also necessary to extend this technique to the trochlear nerve.

Ocular motility review for 1997-1998: part I.

Each year brings new scientific knowledge that builds on itself in a geometric fashion. Ocular motility basic and clinical neurosciences continue to advance with this accelerating pace. The years 1997 through 1998 brought new knowledge to the motility world. This review focuses on the clinical advances within this realm, presented in supranuclear to myopathic organization. Part II of this review will appear in the September 2000 (20:3) issue.

Surgically created fourth-third cranial nerve communication: temporary success in a child with bilateral third nerve hamartomas. Case report.

Shortly after birth, an otherwise healthy infant developed eye deviation and ptosis due to a hamartomatous lesion of the interpeduncular segment of the right oculomotor nerve. The left nerve became similarly involved when the child was 1.5 years of age. Direct nerve repair was not possible. Instead, the trochlear nerve was divided and its proximal end was attached to the distal end of the third nerve. Elevation of the upper eyelid and partial adduction of the eye developed gradually over the ensuing 3 to 5 months. Both functions were lost after an additional 2 months, presumably as a result of tumor recurrence or neuroma formation. This case report shows that surgically created fourth-third cranial nerve communication is feasible and may merit consideration under similar circumstances.

[Changes in subjective cyclodeviation and objective cycloposition after modified Harada-Ito operation in acquired trochlear paralysis]. / Anderungen der subjektiven Zyklodeviation und der objektiven Zykloposition nach modifizierter Harada-Ito-Operation bei erworbener Trochlearisparese.

BACKGROUND: After recently published own investigations on subjective and objective cyclorotatory changes following inferior oblique recession for inferior oblique overaction, it was our aim to determine and to compare subjective and objective cyclorotatory changes following a modified Harada-Ito procedure for acquired trochlear palsy. PATIENTS AND METHODS: Eight patients suffering from acquired uni-(n = 3) or bilateral (n = 5) trochlear palsy were investigated before surgery and 1 day, 3 days and 4 months after surgery. Subjective cyclodeviation was assessed by Harms' tangent scale. Objective cycloposition was measured by means of fundus cyclometry using an infrared Scanning Laser Ophthalmoscope. RESULTS: The immediate postoperative incyclorotatory effect was 12 degrees in the unilateral group and 18 degrees in the bilateral group. Subjective and objective changes were nearly equal in both groups, with a subjective over-effect of 1 degree. After two days of binocular stimulation a marked regression of the surgical effect was found which still increased after four months. The long term incyclorotatory effect was subjectively and objectively nearly equal in the unilateral group which showed a relaps of subjective excyclodeviation of 5 degrees: in the bilateral group, the subjective effect was more pronounced than the objective effect, the immediate postoperative over-effect being disappeared. CONCLUSIONS: In contrast to our results concerning inferior oblique muscle recession for strabismus sursoadductorius, subjective and objective cyclorotatory changes did not differ grossly following a modified Harada-Ito procedure. Subjective and objective short and long term regression was confirmed which objectively exceeded the amount of over-correction. As the underlying cause mechanical and sensory mechanisms are discussed.

The evaluation and treatment of extraocular motility deficits.

Binocular diplopia, monocular diplopia and oscillopsia may be manifestations of skull base lesions or may result from skull base surgery. An ophthalmologic perspective on the diagnosis and treatment of these extraocular motility deficits is reviewed.

[Optic neuropathies and peripheral oculomotor disorders in patients with AIDS]. / Neuropatías ópticas y trastornos oculomotores periféricos en pacientes con SIDA.

In patients with the acquired immunodeficiency syndrome (AIDS) there is an 8% incidence of neuro-ophthalmological changes. The commonest of these neuro-ophthalmological changes are: 1) Cranial nerve pareses 2) Optic neuropathy and 3) Pupil disorders. The cranial nerve pareses are usually combined, rather than single, and are due to intraparenchymatous lesions (toxoplasmosis or lymphoma) or to meningitis (tuberculous or lymphoma). The optic nerve changes tend to be papillitis due to CMV or optic neuropathy due to syphilis or to cryptococcal meningitis. Among the pupil changes, Bernard-Horner syndromes due to sympathetic involvement, Argyll-Robertson pupils due to mesencephalic tectal lesions and mydriasis associated with the common oculo-motor nerve have been described.

Transient trochlear nerve palsy following anterior temporal lobectomy for epilepsy.

Three of 22 patients (14%) who underwent anterior temporal lobectomy for treatment of medically intractable epilepsy at our institution from July 1987 through July 1993 experienced diplopia immediately after surgery. We found ipsilateral paresis of the superior oblique muscle in all three patients. Their ophthalmoplegia resolved completely within 14 weeks. We did not observe any new structural or ischemic changes on postoperative MRIs to account for their deficits. Trochlear nerve palsy--not oculomotor nerve palsy, as is reported in most reference texts--is a relatively common cause of transient diplopia following temporal lobectomy. Indirect (ie, traction) injury of the trochlear nerve is a plausible mechanism that would explain this complication.

Pseudo-Graefe's sign: a manifestation of aberrant regeneration of the fourth cranial nerve?

The phenomena involved in paradoxical upper lid retraction have been observed during recovery from paralysis of the third cranial nerve (CN). One of these phenomena is pseudo-Graefe's sign or Fuch's sign, which is characterized by elevation or retraction of the upper eyelid when the eye is looking downwards and inwards. This synkinesis is caused by an aberrant regeneration of newly formed axons of the third CN that subsequently reach muscles not originally connected with them. Pseudo-Graefe's sign may occur after congenital or acquired diseases. Acquired forms occur more frequently and result from paralysis of the third CN following various intracranial diseases: aneurysms, traumas and tumors.