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Isolated Motor Phenomena and Symptoms of Sleep Handbook of Clinical Neurology, Vol. 99 (3rd series) Sleep Disorders, Part 2 P. Montagna and S. Chokroverty, Editors # 2011 Elsevier B.V. All rights reserved Chapter 54 Isolated motor phenomena and symptoms of sleep R. VETRUGNO, F. PROVINI, AND P. MONTAGNA* Department of Neurological Sciences, University of Bologna Medical School, Bologna, Italy INTRODUCTION Physiological fragmentary (or partial) hypnic myoclonus (PFHM) Sleep identifies a natural and healthy, temporary, and peri- odical state of rest, with suspension of the sensorial func- PFHMs was first described by De Lisi in 1932 as sud- tions of the organs of sense, as well as those of the den, arrhythmic, asynchronous, and asymmetrical brief voluntary and rational soul. Several motor phenomena, twitches involving various body areas, in particular dis- however, occur during sleep, both physiological and tal limb and facial muscles, occurring during sleep. pathological. Such electromyographic (EMG) activity in humans The International Classification of Sleep Disorders, sec- shows an inverse relationship with the degree of sleep ond edition (ICSD-2) (American Academy of Sleep Medi- EEG synchronization (Dagnino et al., 1969), prevailing cine, 2005), lists sleep disorders within eight categories: equally during relaxed wakefulness (nonrapid-eye- movement (NREM) sleep stage 1) and during rapid- I. Insomnias eye-movement (REM) sleep (Montagna et al., 1988). II. Sleep-related breathing disorders The muscle discharges of PFHM appear as isolated or III. Hypersomnias of central origin not due to a circa- bursts of motor unit action potentials with or without dian rhythm sleep disorder, sleep-related breathing visible movement (Figure 54.1). They must originate in disorder, or other cause of disturbed nocturnal the muscle endplate (Buchthal and Rosenfalck, 1966) sleep but are modulated by brainstem regions implicated in IV. Circadian rhythm sleep disorders motor control during sleep. The motor inhibition typi- V. Parasomnias cal of REM sleep is related to state-dependent activity VI. Sleep-related movement disorders of the pontine nucleus pontis oralis which, by exciting VII. Isolated symptoms, apparently normal variants, cells of the medullary nucleus reticularis gigantocellu- and unresolved issues laris, inhibits the alpha motoneurons (Moruzzi, 1972). VIII. Other sleep disorders. A physiological escape from these state-related motor Some periodic and aperiodic phenomena of sleep are inhibition hypothetically accounts for the PFHM, which included within different categories of the ICSD-2, with- is probably caused by descending volleys within the out a unifying classification scheme. Here, these will be reticulospinal system impinging upon the spinal alpha described with their salient characteristics and distin- motoneurons during REM sleep. Indeed, destruction guishing features, ranging from simple movements or of the reticulospinal tract in animals abolished the symptoms of sleep up to more complex behaviors myoclonic activity that remained unchanged by lesion- classified within the parasomnias. ing the dorsal roots, red nucleus, or pyramidal tracts (Gassel et al., 1964). PHYSIOLOGICAL AND EXCESSIVE In humans, PFHM represents a “simple” motor phe- FRAGMENTARY HYPNIC MYOCLONUS nomenon during sleep, present mostly during stage I of NREM sleep and during REM sleep, in apparent con- Myoclonus is part of normal sleep physiology repre- trast with experimental animals which show the highest senting a state-related paradoxical motor excitation. peak of hypnic myoclonic activity during REM sleep *Correspondence to: Pasquale Montagna, M.D., Professor of Neurology, Department of Neurological Sciences, University of Bologna Medical School, Via U. Foscolo 7, 40123 Bologna, Italy. E-mail: [email protected] 884 R. VETRUGNO ET AL. C3–A2 O2–A1 R EOG L EOG Mylohyoideus R orbicularis oculi L orbicularis oculi R masseter L masseter R orbicularis oris 50 µV 1 s L orbicularis oris L tibialis anterior Fig. 54.1. Physiological fragmentary hypnic myoclonus during stage 1 NREM sleep involving face and limb muscles. EOG, electro-oculogram; R, right; L, left. (Gassel et al., 1964). No PFHM was recorded from across a joint space. Similar motor activity during sleep patients with complete peripheral nerve lesions or with has been reported in patients with restless legs syndrome spinal paraplegia. PFHM, absent on the affected side of (Coccagna et al., 1966)(Figure 54.2), in extrapyramidal patients with chronic ischemic hemiparesis and increased syndromes (Tassinari et al., 1965), and in patients with in patients with Parkinson’s disease and Wilson’s disease, REM sleep behavior disorder (Mahowald and Schenck, was normally present in patients with tabe dorsalis in 2000), obstructive and central sleep apnea, narcolepsy, whom muscle proprioception input was probably abol- periodic limb movements during sleep and fatigue ished (Dagnino et al., 1969). A supraspinal origin of (Broughton et al., 1985). EFHM may also present as an PFHM is therefore implicated by its absence in muscles isolated motor phenomenon during relaxed wakeful- that are completely paralyzed because of a peripheral ness, NREM, including stages III and IV, and REM nerve, spinal, or pyramidal lesion, its increase in extrapy- sleep in which “quiver” movements recur throughout ramidal diseases, and by the fact that it remains un- the body, affecting primarily the hands and face with affected by lesions of the dorsal roots that abolish some degree of sleep fragmentation. The twitches may muscle spindle afferent activity. occasionally awake the patient. They are absent during wakefulness and EEG–EMG back-averaging does not show any cortical potentials related to the twitches Excessive fragmentary hypnic (Vetrugno et al., 2002). myoclonus (EFHM) These data suggest a selective impairment of motor EFHM has been reported as a pathological enhance- control during sleep. However, the exact origin and ment of PFHM in which small myoclonic twitches significance of EFHM remain unclear and despite the and fasciculations are present throughout sleep and myoclonus being a common finding in polysomnogra- associated with sleep apnea, excessive daytime drowsi- phy, it is often asymptomatic. EFHM is now classified ness, and insomnia (Broughton and Tolentino, 1984; in the VII section of the ICSD-2 (Isolated symptoms, Broughton et al., 1985; Lins et al., 1993). EFHM may apparently normal variants, and unresolved issues) that cause small movements of the fingers, toes, and/or lists sleep-related symptoms that are in the borderline corners of the mouth, without gross displacements between normal and abnormal sleep. ISOLATED MOTOR PHENOMENA AND SYMPTOMS OF SLEEP 885 C3–A1 O2–A1 Cz–A1 R EOG L EOG Mylohyoideus R wrist extensor R tibialis anterior L wrist extensor L tibialis anterior ECG Intercostalis Oronasal resp. Thoracic resp. Abdominal resp. Plethysmogram Systemic arterial 150 pressure (mmHg) 100 50 100 SaO 2 80 50 µV (%) 60 1 s Fig. 54.2. Excessive fragmentary hypnic myoclonus during stage 2 NREM sleep in a patient with restless legs syndrome. EOG, electro-oculogram; ECG, electrocardiogram; resp., respirogram; SaO2, oxygen saturation; R, right; L, left. HYPNIC JERKS (SLEEP STARTS) and is characterized by the sensation lasting some sec- onds that an explosive noise has occurred in the head, Hypnic jerks, or sleep starts, are normal physiological which wakens the individual from sleep. Patients describe events occurring at the transition from wakefulness to this sensation variously as a terrifying “loud bang” or a sleep, often associated with sensory phenomena, such “shotgun- or bomb-like explosion” (Pearce, 1989), as a feeling of falling, unexplained alarm or fear, inner the most common age of onset being over 50 years. electric shock or light flash (Oswald, 1959; Gastaut and The attacks may have variable frequency, up to more Broughton, 1965). An outcry can occasionally accom- than one per night, for a few weeks or months, with pos- pany the jerks, which are usually associated with auto- sible prolonged or total remissions. Polysomnographic nomic activation (tachycardia, irregular breathing, and studies have documented the occurrence of these attacks sudomotor activation). Jerks consist of nonstereotyped, during all sleep stages, including REM sleep (Sachs and abrupt, and brief flexion or extension movements, Svanborg, 1991), and during the passage from wakeful- generalized, or, more frequently, segmental and asym- ness to sleep (Pearce, 1989). metrical with neck and/or limb muscles involvement. Another related phenomenon at sleep onset, proba- Usually EMG complexes last less than 250 milliseconds bly representing a variant of sensory sleep starts, and are associated with K-complexes and vertex sharp is the Òblip syndrome in which patients experience waves on the EEG (Figure 54.3). momentary sensations of impending loss of con- Hypnic jerks occasionally occur during light sleep, sciousness particularly when relaxed, without any causing a brief arousal. Fatigue, stress, and sleep depri- obvious cardiac, cerebral vascular, or epileptic basis vation may facilitate the occurrence of the hypnic jerks, (Lance, 1996). which may be misdiagnosed as myoclonic seizures. It has been suggested that sleep starts with com- Sleep starts may occur without any motor activity with bined sensory, motor, and autonomic components rep- only visual, auditory, or somesthetic sensory phenom- resent dissociated elements of sleep during which ena. Purely sensory sleep starts without
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