Chronic progressive spinobulbar spasticity with disturbance of voluntary eyelid closure. Report of a case with special reference to MRI and electrophysiological findings

We describe a 56-year-old man who had a progressive pseudobulbar palsy, spastic tetraparesis, forced laughing and disturbance of voluntary eyelid closure, and was clinically compatible with chronic progressive spinobulbar spasticity. Magnetic resonance images (MRI) revealed atrophy of the bilateral motor cortices and single photon emission tomography after intravenous injection of N-isopropyl-p-iodoamphetamine iodine-123 (IMP-SPECT) showed hyporadioactivity in the same regions. Electrophysiological studies on supranuclear paralysis of eyelid closure demonstrated that so-called apraxia and motor impersistence coexisted and that in attempts to keep the eyelid closed the inhibition of basal activity of the levator palpebrae superioris muscle and activation of the orbicularis oculi muscle were insufficient, indicating the impaired reciprocity of these ocular muscles. The corresponding lesion of these eyelid symptoms was considered to be the bilateral motor cortices.     

Dissociation of voluntary eye closure--to keep the eyes closed and to blink--following right hemisphere stroke]

We report a case of a unique eye sign following right hemispheric infarction. This patient was a 78 year old right-handed woman. There was a history of a left hemispheric stroke 1 year previously. On admission, she showed left hemianopia, dysarthria, mild left central facial paresis, bilateral sensory deficit and quadriparesis which were marked on the left side. Babinski sign was elicited on the left. She did not have anosognosia or visual neglect. She had mild orofacial apraxia, but ideomotor and ideational apraxia was absent. There was no motor impersistence. Magnetic resonance imaging of the brain revealed a recent infarction in the territory of the right middle cerebral artery and an old infarction in the left tempro-parietal lobe. The patient could not open her eyelids to verbal command or voluntarily until about two weeks later, when she became able to open her eyes but showed difficulty keeping her left eye closed. She was aware of this problem and could repeat the command and comprehend what was requested to her. On verbal command to close the eyes, her right eye would be closed continuously and excessively and the left eye would only blink. When requested to blink, however, she could blink correctly without excessive eye closure. Spontaneous, reflex and voluntary blinking were normal. Her eyes were closed normally during sleep. Blepharospasm was not seen. The patient showed a striking dissociation between a failure to close her eyes continuously and a preserved ability to blink voluntarily. We suggest that her ability to contract palpebral portion of her left orbicularis oculi muscle is preserved. Regarding the mechanism of the voluntary eye closure system, separate control mechanisms should exist on closing eyes continuously and blinking.     

A case of progressive supranuclear palsy presenting mouth opening difficulty with tonic contraction of the orbicularis oris muscle]

A 72-year-old man developed supranuclear ophthalmoplegia, bradykinesia, rigidity, unsteady gait, dementia, dysphagia, retrocollis, grasp reflex and apraxia of eyelid opening. These findings were compatible with progressive supranuclear palsy (PSP). At the age of 66, he presented a peculiar phenomenon characterized by simultaneous tonic contraction of the orbicularis oris muscle (OOM) and the palatal muscles elicited by pronouncing "pa", which resulted in difficulty of voluntary opening of the mouth and the rhinopharynx. Therefore, the respiration air reciprocated between the lung and the closed mouth. The expiratory pressure puffed out the cheeks, while the lips remained tightly closed. While the respiratory movements and the pressure increased by degree, the OOM contracted more strongly in proportion to the pressure. Sixty to ninety seconds after the elicitation, the pressure overcame the contraction of the OOM and the course of the phenomenon was completed. The electromyograms showed that the OOM activity was prolonged after initial voluntary contraction, remaining thus after a tracheostomy for pneumonia at the age of 72, and that it increased in response to the pressure. Apraxia of eyelid opening, one of the other symptoms, resembled this phenomenon in terms of the aspect of difficulty of voluntary mouth opening. The "holding" phase of grasp reflex, yet another symptom, resembled it in the recruitment of the OOM activity. The phenomenon is not common in patients with PSP. However, we concluded that it may be included among the symptoms of PSP because it has similar characteristics to apraxia of eyelid opening and grasp reflex, which are not uncommon in patients with PSP.     

The relationship of eyelid movement to the blink reflex

Although the blink reflex is a standard neurophysiological investigation its relationship with eyelid movement has not been clearly established. We studied normal subjects and patients with unilateral facial paralysis to define the pattern of eyelid movement following glabellar tap, supraorbital nerve stimulation, facial nerve stimulation and direct corneal stimulation. We found that eyelid closure did not necessarily occur in a single movement. Following glabellar tap the first component of a two-stage movement was initiated by levator palpebrae relaxation while with supraorbital nerve stimulation orbicularis oculi contraction produced the first movement. The compound muscle action potential following direct facial nerve stimulation produced only minimal eyelid movement, the major closure being associated with a longer latency orbicularis oculi reflex. Corneal stimulation elicited a single component eyelid movement. Thus, the pattern of eyelid movement differed for each stimulus reflecting variations in orbicularis oculi contraction and levator palpebrae inhibition.     

Apraxia of eyelid closure in Huntington's disease

Summary. We report a patient with genetically confirmed Huntington's disease (HD) presenting apraxia of eyelid closure (AEC). She was unable to close her eyes at command but was able to blink. Chorea and AEC ameliorated significantly during treatment with olanzapine and riluzole, an inhibitor of glutamate release. AEC is reported in progressive supranuclear palsy, Creutzfeldt-Jakob's disease, amyotrophic lateral sclerosis, and as post-stroke AEC. No report on HD is available so far, although oculomotor disturbances are quite common in this disease. Received September 5, 2001; accepted December 5, 2001     

Eyelid movements in health and disease. The supranuclear impairment of the palpebral motility.

The eyelid movements are mediated mainly by the orbicularis oculi (OO) and the levator palpebrae superioris (LPS) muscles. Dissociated upper lid functions exhibit different counterbalanced action of these muscles, and in blinking they show a strictly reciprocal innervation. The disturbance of this close LPS-OO relationship likely leads to many of the central lid movement disorders. Three groups of supranuclear motor impairment of lid movements are considered: the disorders of the lid-eye movements' coordination, the disturbances of blinking and lid "postural" maintenance, and the alteration of voluntary lid movements. Nuclei of the posterior commissure control the inhibitory modulation of LPS motor-neuronal activity and they are involved in the lid-eye coordination disorders such as lid retraction, which is observed in the Parinaud's syndrome and also in parkinsonism and progressive supranuclear palsy. Spontaneous (SB) and reflex blinking consist of two components: the inhibition of the basal tonic LPS activity, which keeps the eyes open, and the concurrent activation of the OO muscles. LPS inhibition precedes and outlasts the OO activation. This normal configuration is impaired in parkinsonism and blepharospasm (BSP). SB shows a highly interindividual rate variation (among 10-20 per minute in adults) and abnormal blink rates occur in neurological diseases related to dopaminergic transmission impairments. Lid postural abnormalities include involuntary eyelid closure, which is usually associated with inability to open the eyes. Two major disorders share these two aspects: BSP and blepharocolysis (BCO). BSP consists of an involuntary overactivity of the OO, with LPS co-contraction activity, and is expressed as frequent and prolonged blinks, clonic bursts, prolonged tonic contraction or a blend of all of them. BCO (commonly named "so-called lid opening apraxia") is an overinhibition of the LPS with no evidence of ongoing OO activity. BSP and BCO occur in many instances of idiopathic dystonias and basal ganglia diseases and, less frequently, in rostral brainstem lesions. Both may coincide in the same patient. Voluntary lid movement disorders comprise the impairment of Bell's phenomenon, the voluntary eyelid closure palsy and the so-called cerebral ptosis, all related to lesions of frontal cortical areas and/or the corticospinal system.     

Right-left dissociation of voluntary eyelid closure following right middle cerebral artery infarction

We encountered two patients with right middle cerebral artery infarction who showed a unique eye sign not described so far. Both had suddenly developed central facial weakness, hemiplegia and hemisensory deficit in the left side. Anosognosia for the left hemiplegia, motor impersistence and left unilateral spatial neglect were also present. Initially they showed difficulty in keeping their eyes closed to the same degree on both eyes. However, this symmetrical motor impersistence of eye closing developed into a differential pattern over the days. Thus, on verbal command to close the eyes, the right eye in the non-paretic side would be closed continuously and excessively and in the left eye in the paretic side would be closed slightly and impresistently. This dissociation of eye closure was not observed in spontaneous eye closure. This symptom is close to the contralateral motor impersistence of eye closure which has been attributed to the right hemispheric lesion. But the concurrence of the ipsilateral overcontraction of the orbicularis oculi has not been described to the authors' knowledge. We proposed a hypothesis on this unique right-left dissociation of eye closing behavior.     

Involuntary closure of eyelids in parkinsonism. Electrophysiological evidence for prolonged inhibition of the levator palpebrae muscles

Involuntary closure of eyelids (ICE), a phenomenon variously interpreted as blepharospasm and apraxia of lid opening, is occasionally observed in parkinsonism. Nine patients (4 with Parkinson's disease, 2 with post-encephalitic parkinsonism, and 3 with supranuclear palsy) with prominent ICE, were studied by electromyographic recording of the eye muscles. ICE episodes were shown to be dependent upon prolonged, irregular inhibition of the normal tonic activity of the levator palpebrae superioris (LPS) muscle causing drooping of the upper eyelid without any corresponding activation of the orbicularis oculi (OO) muscle. Nevertheless, some degree of excessive, widely fluctuating OO activity was present in seven of the patients. Blepharocolysis (from Gr. blepharon, eyelid, and kolysis inhibition) is put forward as the term to designate ICE episodes resulting from abnormally long inhibition of the LPS muscles and should be differentiated electrophysiologically from blepharospasm, excessive OO muscles activity. Abnormal influences from basal ganglia acting on brainstem structures that regulate blinking may falicitate either of the two components of normal blinking resulting in ICE due to the predominance of LPS inhibition (blepharocolysis), the predominance of OO activation (blepharospasm) or a combination of the two.     

Gaze-evoked eyelid closure. Report of two cases

Various types of associated movements of eyeballs with other cranial muscles have been described in the literature. Only a few observations, however, have been reported on the relation of ocular movements and facial muscles innervated by the facial nerve, especially the orbicularis oculi muscles. We report two cases presenting gaze-evoked involuntary contraction of the orbicularis oculi muscle and unilateral eyelid closure. Case 1 was a 38-year-old housewife who was admitted to our hospital because of gait disturbance and sensory deficits below the neck. She had a 5-year history of left facial palsy, disturbed horizontal eye movements, retrobulbar optic neuritis, spastic paraparesis and bladder and rectal disturbances, some of which had relapsed a few times. Neurological abnormalities were summarized as follows: bilateral pale discs, right Horner's sign, horizontal nystagmus, left facial nerve palsy of peripheral type, spastic paraparesis with left-sided predominance, sensory disturbances below the third cervical segment, truncal and limb ataxia, and bladder and rectal disturbances. Gaze-linked synchronized contraction of the left facial muscles was observed and on the left lateral gaze marked spasm of the left orbicularis oculi muscle with occasional lid closure was evoked. Case 2 was a 72-year-old female with cerebellar hemorrhage. Neurological abnormal findings included mild disorientation, meningeal irritation signs, horizontal nystagmus on lateral gaze, reduced response of reflex eye movement to the left, minimal weakness of the left facial muscles, ataxic dysarthria, mild left hemiparesis and hemisensory deficits with face, truncal and limb ataxia. She could move eyeballs to any direction but with effort to the left.(ABSTRACT TRUNCATED AT 250 WORDS)     

Stretch reflex blepharospasm

We studied a patient with blepharospasm provoked by stretching the orbicularis oculi muscles. With the eyes closed, EMG of the orbicularis oculi at rest revealed spontaneous rhythmic muscle activity that was not visible. When she tried to open her eyes, repetitive jerking blepharoclonus and tonic blepharospasm rendered her functionally blind. Passive stretching of the orbicularis oculi evoked a burst of EMG activity with two components. Touch or pinprick did not elicit such reflex activity. Anesthesia of the supraorbital nerves abolished muscle responses to stretch and improved the blepharospasm.     

建立人工面神经反射弧恢复失神经支配眼轮匝肌的闭眼功能

目的：建立人工面神经反射弧,恢复面瘫兔的闭眼功能。 方法：试验动物为新西兰兔12只。采用手术切断面神经制备单侧周围性面瘫模型,患侧行肌电图检查确诊。术后第5天患侧植入刺激电极,健侧植入采集电极并留置1月。患侧分别于术后第7天、第28天给予电流刺激;而健侧采集电极则连续采集2周的肌电信号。建立健侧眼轮匝肌肌电信号采集、中枢信号处理模式识别、患侧电流刺激眼轮匝肌系统。当健侧眼轮匝肌采集的肌电信号经信号识别、提取以及电脑分析判断,符合其闭眼刺激阈值时,即对人工电刺激器发出指令,由刺激电极直接作用于患侧眼轮匝肌,引起眼睑完全闭合。结果：刺激方式为正负方向矩形波,电流强度为0.40—0.70mA之间可引起患侧眼轮匝肌收缩,眼睑完全闭合。当健侧眼睑闭合时,其肌电信号电压大于50uV,触发电刺激器,电流刺激即引发患侧眼轮匝肌收缩,完成眼睑闭合。结论：利用MEMS技术,在面瘫兔模型建立“人工面神经反射弧”,恢复患侧眼轮匝肌闭眼功能。     

"Apraxia" of eyelid opening: an involuntary levator inhibition

Apraxia of lid opening was described by Goldstein and Cogan as "a non paralytic motor abnormality characterized by the patient's difficulty in initiating the act of lid elevation." We studied six such patients with this finding accompanied by vigorous frontalis contraction and no evidence of ongoing orbicularis oculi contraction, dysfunction of the oculomotor nerve, or loss of ocular sympathetic innervation. Four patients had Parkinson's disease or atypical parkinsonism, one had progressive supranuclear palsy, and one had Shy-Drager syndrome. At onset of ocular symptoms, mean age was 64 years, and the mean duration of extrapyramidal symptoms was 9.7 years. By definition, the motor system must be intact in any apraxia. Therefore, this disorder of lid opening in patients with extrapyramidal motor dysfunction is not an apraxia, but rather involuntary levator palpebrae inhibition of supranuclear origin.     

A 77-year-old man with gait and gaze disturbance]

We report a 77-year-old Japanese man with progressive gait disturbance. He was well until his 71 years of the age (1992), when he noted an onset of disturbance in his speech, which was followed by difficulty in using his left hand. He did not attempt to use his left hand afterwards. He started to fall down in the spring of 1994. He was admitted to our service on October 6, 1994. Neurologic examination revealed an alert and oriented man. He showed limb-kinetic apraxia in his left hand with anosognosia for his apraxia. Vertical gaze was impaired. He walked in small steps. He had moderate axial and limb rigidity. He had no weakness, ataxia, or tremor. Deep tendon reflexes were normal. Plantar response was flexor. Sensation was intact. His gait had progressively become worse and he was admitted to another hospital in April of 1996. At that time he was disoriented to time. He was only able to walk a few steps with support. He continued to show limb-kinetic apraxia in his left hand. He developed dementia and dysphagia and he expired on October 27, 1998. He was discussed in a neurological CPC, and the chief discussant arrived at the conclusion that the patient had corticobasal degeneration. Most of the participants agreed with this diagnosis, but a few of them thought that progressive supranuclear palsy would be more likely. Post-mortem examination revealed no gross cortical atrophy. The right hemisphere was kept frozen for future biochemical analysis. The left precentral gyrus showed spongy changes, neuronal loss and gliosis. The pallidum, putamen, and the subthalamic nucleus were unremarkable, however, neurofibrillary tangles were seen in the subthalamic nucleus. The substantia nigra showed only slight neuronal loss; neuronal pigments were well retained. A few neurofibrillary tangles were seen in the remaining neurons. The cerebellar dentate nucleus showed grumose degeneration. Gallyas-Braak staining revealed many tuft-shaped astrocytes in the precentral gyrus. Pathologic diagnosis was progressive supranuclear palsy. Some participants thought that this diagnosis was unacceptable, because the pathologic changes in the substantia nigra, globus pallidus, and the subthalamic nucleus, which were usually severely involved in PSP, did not show typical changes of PSP. In addition, the predominant clinical feature was limb-kinetic apraxia, although he showed vertical gaze paresis and parkinsonian gait, which could also be seen in corticobasal degeneration. There was a big discussion among participants with regard to the diagnosis.     

Voluntary eyelid contraction modifies the blink reflex recovery cycle

In order to determine the extent to which the recovery cycle of the blink reflex is modified by voluntary contraction of the eyelids we investigated the electrically elicited blink reflex with paired stimuli of identical intensity in 9 healthy subjects. We pseudorandomly administered two interstimulus intervals (150 ms and 250 ms) in three different conditions of voluntary contraction of the orbicularis oculi muscle (relaxed, mild lid closure and strong lid closure). Our results show that inhibition of the R2 response following the second stimulus is significantly reduced with voluntary contraction. In addition, we found significantly larger amplitudes and shorter latencies of R1 and R2 with voluntary contraction. We conclude that in healthy subjects, voluntary eyelid contraction causes facilitation or disinhibition not only in the nuclei of the seventh cranial nerve, but also in the polysynaptic pathway of the R2. The possible implications on the interpretation of clinical data are discussed.     

Regional differences in the orbicularis oculi muscle: conservation between species.

The orbicularis oculi muscle is a complex facial muscle involved in eyelid closure. The central parts of pretarsal and preseptal regions of the palpebral part of the orbicularis oculi muscle in rabbit and cynomolgus monkey lower eyelids were examined histologically and were analyzed for muscle fiber number, muscle fiber cross-sectional area and fiber type composition. Distinct regional differences were seen in the muscle fiber composition in these two regions of the muscle. The pretarsal portion of the muscle, that closest to the eyelid margin, was quite homogeneous and almost completely composed of type 2 fibers. These fibers were the smallest in cross-sectional area. Type 2 fibers also predominated in the preseptal portion of the muscle, but this region contained between 10 and 20% type 1 fibers. They appeared to be a gradient in muscle fiber size, whereby the fiber size increased as a function of the distance from the eyelid margin. The same pattern of regional differences were found in both rabbit and monkey orbicularis oculi. Thus, there is a clear conservation of these regional differences in these two species. While the developmental significance is unknown, the identification of this pattern may facilitate the evaluation of chemomyectomy agents for treatment of eyelid spasms in humans and allow a more accurate analysis of biopsy material from this muscle.     

Eyelid movement abnormalities in progressive supranuclear palsy

We systematically videotaped eyelid movements in a community-based series of 38 patients with progressive supranuclear palsy (PSP). Ten patients (26%) had blepharospasm, "apraxia" of lid opening and/or "apraxia" of lid closing. These patients as a group had more severe upgaze paresis but no greater disease duration than the patients without supranuclear lid dysfunction. Patients used a variety of synkinetic movements to overcome lid-movement abnormalities. One patient displayed "slow blinks," a phenomenon not previously described in PSP. Blink rate in PSP, 3.0/min, was markedly lower than that in patients with Parkinson's disease (PD), 12.5/min, and patients with PSP but not PD increased their blink rate during command versional eye movements.     

An apraxia of eyelid closure in association with frontal lobe atrophy in a patient with amyotrophic lateral sclerosis]

A 57 year-old woman with amyotrophic lateral sclerosis (ALS) and an apraxia of eyelid closure was reported. Her first symptom was muscle weakness in the right arm. Since neurological examination showed mainly upper motor neuron sign with neurogenic pattern in the needle electromyograms of the tongue and limb muscles, she was diagnosed as ALS. Two years and 6 months later from onset, she showed an inability to close her eyelids voluntarily or on command with normal reflex closure. MRI of the brain showed atrophy in the frontal lobe and anterior of the temporal lobe, where 123 I-IMP SPECT revealed hypoperfusion. Considering previous reports, there might be an ALS subset who showed atrophy of frontal lobe together with apraxia of eyelid closure.     

Botulinum toxin injection into Riolan's muscle: somatosensory 'trick'

We studied the effect of injecting botulinum toxin A (BTX-A) into the pars ciliaris--also known as Riolan's muscle--of patients with eyelid apraxia (ELA). Six patients with ELA were treated with injections of BTX-A into the region of Riolan's muscle at the medial and lateral portions of the upper and lower pretarsal orbicularis oculi. Clinical benefit was seen in all 6 patients, 2 of whom had previously been treated with conventional pretarsal injections of BTX-A and had not improved. BTX-A injections into Riolan's muscle are effective as treatment for ELA. The proposed mechanism is not that of muscle relaxation but rather modulation of the somatosensory cortex, similar to that of a 'sensory trick' in patients with dystonia.     

Thixotropy of levator palpebrae as the cause of lagophthalmos after peripheral facial nerve palsy

Patients with facial nerve palsy are at risk of developing corneal ulceration because of lagophthalmos (incomplete closure of the affected eyelid). Lagophthalmos could result from thixotropy of the levator palpebrae muscle--that is, the formation of tight crossbridges between the actin and myosin filaments of the muscle fibres causing stiffness of the muscle--rather than from paralysis of the orbicularis occuli muscle as previously supposed. This possibility was investigated in 13 patients with a peripheral facial nerve palsy in a prospective open study. The levator muscle of the affected eyelid was stretched by manipulation and downward movement of the passively closed upper eyelid for approximately 15 seconds. The amount of lagophthalmos was measured before and immediately after this manoeuvre. In all patients except one there was a clear reduction in lagophthalmos (mean reduction 72%; range 60-100%). Thus in this setting the lagophthalmos appears to be caused by thixotropy of the levator palpebrae muscle, which has implications for treatment.     

A silent period in orbicularis oculi muscles of humans.

Surface electromyographic activity was recorded bilaterally from orbicularis oculi muscles when subjects relaxed and contracted eyelid muscles. Cutaneous reflex responses were evoked during both the relaxed and contraction states. Following reflex elicitation periods of muscle silence in orbicularis oculi were observed for about 10 to 15 ms after the ipsilateral R1 response and for up to 100 ms after the bilateral R2 responses. Reflex responses appeared to be enhanced when elicited during contractions. Possible physiological mechanisms are discussed regarding the presence of silent periods in a motor system that is presumably devoid of spindles, Golgi tendon organs, and Renshaw-like interneurons.