Relationship of Periodic Movements in Sleep (Nocturnal Myoclonus) and the Babinski Sign

Transcription

1 Sleep. 8(3): Raven Press. New York Relationship of Periodic Movements in Sleep (Nocturnal Myoclonus) and the Babinski Sign Robert C. Smith Sleep Disorders Center. St. Louis University. St. Louis, Missouri, USA Summary: To obtain a comprehensive clinical description of periodic movements in sleep, the first 11 videotaped movements of nine patients were studied. These leg movements were characterized by active dorsiflexion of the ankle (91%), dorsiflexion and fanning of the small toes (82%), and dorsiflexion of the great toe (72%). Partial flexion of the knee and hip occurred in 28%. Simultaneous dorsiflexion of the ankle and small toe was almost always the initial change, either preceding or occurring simultaneously with extension of the great toe. Knee and hip flexion almost always followed foot movements. Tonic and/or clonic movements, usually about the ankle, occurred in 75%; plantar flexion of the ankle occurred in 21% at the end of a leg movement. Periodic movements in sleep were thus characterized on detailed videographic analysis by movements similar to the Babinski response. Since both the normally occurring nocturnal Babinski response and periodic movements in sleep are also almost entirely NREM related, the author proposes that periodic movements in sleep are due to the NREM loss of supraspinal inhibitory influences on the pyramidal tract and that the characteristic foot and leg movements are Babinski-type responses secondary to this. Key Words: Periodic movements in sleep-nocturnal myoclonus-babinski sign Pyramidal tract disease. Current definitions of periodic movements in sleep (PMS) specify that the leg movements are characterized by rapid partial dorsiflexion of the ankle, extension of the great toe, and partial flexion of the knee and hip (1,2). Although common, PMS is of uncertain origin and significance (3) and has been reported in association with many different sleep disorders and asymptomatic states (2,4). Although careful clinical observations of PMS have been reported, including cinematographic analyses 0), the major emphasis has been on the polysomnographic characteristics of these foot and leg movements (5). The present study used videographic techniques in nine patients with PMS to make detailed observations of their foot and leg movements. The findings corroborated, and slightly expanded, earlier clinical descriptions and led to the hypothesis that periodic movements in sleep are Babinskitype responses due to changes in the pyramidal tracts during NREM sleep. Accepted for publication May Address correspondence and reprint requests to R. C. Smith at Division of General Internal Medicine, Department of Medicine, Michigan State University College of Human Medicine, East Lansing, MI 48824, U.S.A. 239

2 240 R. C. SMITH METHODS Eight of the subjects were referred to the St. Louis University Sleep Disorders Center with the following primary sleep complaints: insomnia (n = 3), snoring (n = 2), and possible obstructive apnea (n = 3). One subject was a volunteer student. The evaluation of each patient consisted of a medical and sleep history and a physical examination. Each had a nocturnal polysomnogram which included the central (C3) and occipital (01) electroepcephalograms, electro-oculogram, submental electromyograms (EMG), and bilateral anterior tibial EMGs. Some also had nasal/oral airflow recorded with a thermistor. Sleep stages were scored according to the guidelines of Rechtschaffen and Kales (6). Videographic study, performed with a video camera in the patient's room, was controlled by a technician in an adjoining room to avoid disturbing the patient. Evaluation of the videotapes, at slow and normal speeds, was performed by the author to rate the nocturnal movements of the single foot and leg that could be captured on the videotape. RESULTS Nine Caucasian patients, six men and three women, mean age 41 years (range years), were studied. The 9 subjects represented all patients suspected of having PMS for whom adequate videotaping of the nocturnal leg movements could be obtained during a 6- month period. Eight of the patients met Association of Sleep Disorders Centers' criteria for nocturnal myoclonus while one patient had only two trains of myoclonus. There was suspicion of nocturnal myoclonus in three patients and restless legs in five. Nocturnal myoclonus was the primary diagnosis for the sleep disorder in four, a contributing factor in two, and non-contributory in three patients. Other primary sleep-related diagnoses were sleep apnea, insufficient sleep, and underlying medical conditions, i.e., one patient had undergone craniotomy and had, on neurologic examination, only a visual field defect; another patient had incurred a brain stem stroke resulting in isolated right-sided Horner's syndrome. The remaining seven patients had no neurologic disease nor abnormalities on physical examination. Only the first 11 movements, all from NREM, in each of the nine cases were rated (range movements, mean 17.3). Although there was considerable variability within and among patients some common features of the periodic leg movements were observed. The great toe was actively dorsiflexed in only 72 of 99 periodic leg movements (range per case 3-11) evaluated, while the ankle actively dorsiflexed in 91 of 99 movements (range per case 3-11). Active dorsiflexion (with fanning) of the four small toes occurred in 82 of 99 movements, almost always simultaneously with ankle movement. Flexion of the knee and hip occurred in only 28 of 99 movements (range per case 0-11), with no motion at all in five cases. The sequence of foot movements showed three common patterns: ankle and small toe movement alone (32 of 99 movements); ankle and small toe movement followed by great toe movement (27 of 99 movements); ankle, small toe, and great toe movement simultaneously (27 of 99 movements). The great toe preceded the ankle and small toes in only 2 of 99 movements. Movement of the ankle alone (2 of 99 movements), great toe and ankle (1 of 99 movements), and knees and hips alone (8 of 99 movements) accounted for the remainder. When movement of the knees and hips was associated with foot movement (20 of 99 movements), it followed in 18 of 20 movements and preceded in 2 of 20 movements. Repetitive up-down (clonic) foot movements, usually represented on EMG as typical single leg movements, were the rule; only 1 of 9 cases showed no clonus. There was a total of 55 of 99 repetitive movements. The mean number of repetitions was 2.8, involving the

3 PMS AND THE BABINSKI RESPONSE 241 ankle in 7 of 8 cases and the great toe in 1 of 8 cases. Tonic movements, defined as either sustained dorsiflexion or delay in relaxation following dorsiflexion, occurred in 34 of 99 movements, involving the ankle and small toes in 6 of 7 cases and the great toe in 1 of 7 cases. Twenty of 34 tonic movements occurred where there had been no clonic movements, so that a total of 75 of 99, including all patients, exhibited tonic and/or clonic foot movements. Plantar flexion occurred in 21 of 99 movements at the end of the foot movements. Of the five cases exhibiting this, four occurred with the ankle and small toes and one involved the great toe. DISCUSSION An active tonic/clonic dorsiflexion of the ankle and toes best describes the periodic movements of sleep reported here, while flexion of the knees and hips was much less prominent. Dorsiflexion of the ankle and small toes was almost always the initial movement, at times accompanied by dorsiflexion of the great toe. There were important limitations to the study, however. A larger population and independent rating would have enhanced the findings. Direct electrophysiological confirmation of the many observed movements (from the extensor halluc is longus, flexor halluc is brevis, tibialis anterior, and extensor digitorum longus, for instance), although difficult to obtain because of their invasive nature, would have been useful in verifying the number and sequence of these rapid foot movements. Study of patients at different times of night, on different nights, and of both legs will be important in future studies. Nevertheless, the study was consistent with descriptions by both Guilleminault (1) and Coleman (2). Lugaresi (7) also emphasized clonic activity in conjunction with what he defined as the closely related restless legs syndrome. The author was intrigued by the similarity of these foot and leg movements to the abnormal plantar response (Babinski sign) that is elicited by stroking the lateral aspect of the sole during wakefulness. The present study shows that periodic movements in sleep are consistently described by the same features that characterize the Babinski response: dorsiflexion of the ankle, small toes (with fanning), great toe, and, at times, flexion of the knee and hip (8). The Babinski response elicited during wakefulness is a reliable index of pyramidal tract disease. It is thought to be a spinal polysynaptic reflex that is inhibited in normal people by descending impulses in the pyramidal tract (9,10). The Babinski response has also been observed as a normal and temporary phenomenon in other situations, such as in the newborn where its gradual disappearance parallels myelinization of the pyramidal tracts (9,11). This response is also found normally during recovery from general anesthesia, which is thought to inhibit supraspinal control of the reflex mechanism (12-15). Of more importance to the present study is that the Babinski response to plantar stimulation has been reported as a normal occurrence during NREM sleep (9,16,17). Fujiki et al. (9) studied 14 normal patients in whom a waking Babinski sign was not elicited. Seven of 14 exhibited a Babinski sign during NREM sleep while there was only one equivocal response during REM. Three patients with transverse spinal lesions and waking Babinski signs exhibited a Babinski response to plantar stimulation in REM as well as NREM. It was concluded that this common NREM phenomenon was due to depression of waking inhibitory supraspinal influences during NREM that were, however, not depressed in normal subjects during REM. It can be concluded, therefore, that the leg movements in PMS not only resemble a Babinski response, but occur under the same temporary circumstances of NREM sleep (3) which characterize a normally occurring nocturnal Babinski response. There is further

4 242 R. C. SMITH clinical evidence that PMS and the Babinski response may be closely related. The high incidence of clonus in the present study is indicative of pyramidal tract involvement in PMS, further supporting the contention that the leg movements are related to NREM changes in pyramidal tract function. Moreover, if the response to general anesthesia is considered as a model for understanding varying degrees of pyramidal tract suppression, clonus is found to be the step following the appearance of the Babinski response during recovery from general anesthesia (14,15). This indicates the close association between the two during another type of temporary pyramidal tract suppression. The hypothesis that the leg movements of PMS are Babinski-type responses occurring without plantar stimulation suggests a central origin of PMS (3). This hypothesis is also consistent with other neurologic changes in PMS of probable central origin, i.e., periodicity of the leg movements (18), their association with K-complexes (7), and varying occurrence of the movements from one leg to the other or in both. In addition, reflex activity has been reported to be selectively altered during sleep. Not only is the Babinski response depressed in REM (17), but there is also selective depression of the monosynaptic spinal H-reflex in humans during REM (19), thought also to be due to descending supraspinal influences (20). Both monosynaptic and polysynaptic reflexes in the cat are depressed in REM (9). This hypothesis suggests that a commonly occurring biologic phenomenon, NREM suppression of inhibitory suprasegmental influences, may be an important predisposing factor for the development of PMS, and that individual vulnerability to PMS most likely varies. Thus, the 50% of Fujiki's patients who had nocturnal Babinski responses (9) would be predicted to be more susceptible. This common loss of NREM supraspinal control could predispose many individuals to develop either a spontaneously occurring Babinski-like response or one that occurs from minimal stimulation of the foot or other body part (10,13). More important than these implications, however, is that the hypothesis itself is in need of further exploration and testing. Acknowledgement: The author wishes to thank Janice Weiss, Jeff Sevier, and Janice Herrmann for their invaluable advice and tireless assistance. REFERENCES I. Guilleminault C, Raynal 0, Weitzman ED, Dement WC. Sleep-related periodic myoclonus in patients complaining of insomnia. Trans Am Neural Assoc 1975;100: Coleman RM, Pollack C, Weitzman ED. Periodic movements in sleep (nocturnal myoclonus): relation to sleep-wake disorders. Ann Neural 1980;8: Coleman RM. Periodic movements in sleep (nocturnal myoclonus) and restless legs syndrome. In: Guilleminault C, ed. Sleeping and waking disorders: indications and techniques. Menlo Park, CA: Addison Wesley Publications, 1982: Bixler E, Soldatos R, Scarone S, Martin E, Kales A, Charney D. Similarities of nocturnal myoclonic activity in insomniac patients and normal subjects. Sleep Res 1978;7: Association of Sleep Disorders Centers, Diagnostic Classification of Sleep and Arousal Disorders, First Edition, prepared by the Sleep Disorders Classification Committee, HP Roffwarg, Chairman. Sleep 1979;2: Rechtschaffen A, Kales A, eds. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Washington, DC: Public Health Service, US Government Printing Office, Lugaresi E, Coccagna G, Berti-Ceroni G, Ambrosetto C. Restless legs syndrome and nocturnal myoclonus. In: Gastaut H, Lugaresi E, Berti-Ceroni G, Coccagna G, eds. The abnormalities of sleep in man: proceedings of the 15th European meeting on electroencephalography, Bologna, Bologna: Aulo Gaggi Editore, 1968: Grinker RM, Bucy PC, Sahs AL. Neurology. Springfield, IL: Charles C. Thomas, Fujiki A, Shimizu A, Yamada Y, Yamamoto J, Kaneko Z. The Babinski reflex during sleep and wakefulness. Electroenceph Clin Neurophysiol 1971;31:

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