H Lauerma

I Lehtinen

J A Korkeila

K Vaahtoranta

P Lehtinen

R Holmström

S Toivonen

English

UTUPub

BIOL PSYCHIATRY 191 1992;32:191-194 Laterality of Motor Activity During Normal and Disturbed Sleep Hannu Lauerma, Ilkka Lehtinen, Piiivi Lehtinen, Jyrki A. Korkeila, Sauli Toivonen, Kaarlo Vaahtoranta, and Reijo Holmstr6m Introduction In a review, Gardner and Grossman (1976) dis- cussed the possibility that small and large sleep movements may be of different neural origin. Small, usually distal, twitches are possibly due to bursts of spinal disinhibition, whereas large movements are mort. likely caused or timed by afferent stimuli. Jovanovic (1971 ) found that daring sleep the nondominant hand is moved twice as much as the dominant, independent of the REM/NREM cycle. Nondominant hand mevements while awake have been shown to reflect higher cerebral functions, spatial rather than verbal problem solving (Hampson and Ki- mura 1984), and possibly the personal use of visual imagery in verbal encoding (Sousa-Poza et al 1979). The significance of~Ie iiohdominant activity for the psychophysiology of sleep is unclear becw.u,e the laterality might be due to the preferred right-side sleeping posture. Move- mel,~t activity might also consist of typical left hz~nd movemei~t~, thus reflecting no difference in activity between wakefulness and sleep. Many subtle forms of deviant lateralizntion From the Psychiatric Clinic (ilL, PL, JAK, RH) and Department of Physiology (IL, ST, KV), University of Turku, F'mland, Adda~ relahtt ngluests to Haanu Lauenna, M.D., Psychiatric Clinic, Turktt City ilospital, Kunnallissairaalant. 20, SF-20700 'rurku, Finland. Received February !0, 1992; revised May 26, 1992. The pre!iminary results without statistical analysis and thorough theoretical fommlation were initially laesented as an oral im'sen- tafion in the 9th European Congress of Sleep Research, Jen, salem, September 9, 1988 by HI.. have been found in psychiatric syndromes. Phe- nomenologically dose to mental and physical aspects of panic disorder are consistent left.sided symptom findings in conversion symptoms (Galin et al 1977) and hyperventilation (Blau et al 1983). Deviant motor activity may be a fundamental feature of sleep disturbance in psychb, tric dis- orders (Foster and Kupfer 1975; Kronholm and Hyyppii 1987) but little is known about the na- ture of these movements. In order to character- ize movement activity in the sleep of panic dis- order patients, and to test the hypothesis of different neuronal origin of small and large movements, we chose to examine their lateral distribution. Materials and Methods The unilateral head movements of nine patients suffering from panic disorder (PD) and hyper- ventilation syndrome (seven men, two women, aged 29-56 years, mean 44.6 years) and nine age-matched and gender-matched nurmal con- trois, were counted by infrared video recording and a Static Charge Sensitive Bed (SCSB). The SCSB is a sensitive and reliable movement de- tector. It has the unique ability to detect the smaflest movement, as a motor event exceeding three times the amplitude of the ballistoeardi- ogram, which is seen as background activity in the movement channel of the SCSB (Alihanka 1987; Polo et al 1991). The patients were re- fened from other hospital departments because of negative findings in medical and neurological © 1992 Society cf Biologic~ Psychiatry 0,306-_ 3223/9~/$05.00 192 BIOL PSYCHIATRY Brief Reports 1992;32:191- lea examinations, and suspicion of hyperventilation syndrome or PD. The diagnosis of PD was made after psychological and psychiatric interviews using a symptom checklist filled out by the pa- tient, in accordance with the DSM-LII criteria. They had not previously been treated for PD, althoug h six of them had occasionally used mi- nor tranquilizers. The duration of symptoms ranged from 4 months to 12 years, median 2 years. The selected patient sample reflects the combination of many factors, such as patient compliance and laboratory availability. The control subjects, six men, three women (age range 25-54 years, mean 36.1 years) were non- paid, voluntary acquaintances of the laboratory staff. A 10th male control subject was examined polygraphicaily (Table 1). Each subject reported negative history of left handedness in childhood, and used the right hand in writing, drawing, and hammering. All subjects were instructed to re- frain from medications and alcohol for a mini- mum of 48 hr before the first night (i.e., 96 hr before the polygraphy). The subjects gave their informed consent. On the first two nights only telemetric elec- trocardiograph (ECG) cables were attached to the st:bject. On the third night, the standard polygraphy electroencephalogram (EEG), elec- tromyogram (EMG) and electrooculograph (EOG) were used. To make sleeping conditions as natural as possible, normal bed clothes were used: This posed a problem for analysis of movement, but helped the subject to feel nor- mally relaxed, and :emoted natural behavior. The screening of both the video SCSB graphs and the subject toged~er provided a highly ac- curate and detailed analysis of the motor activ- ity. The movements can be analyzed in less 61an real time as the videotape can be. operated on "fast-forward" most of the time without losing any movement. Movements made during dif- ferent stages of sleep and during wakefulness were first classified according to how well or- ganized they seemed to be. The scorers who counted the movements were blind to the sub- jects' handedness and sleep stage. Because of low interrater correlation, the maiil source of which were problems in classifying the more complex movement patterns (e.g. during pos- tural shifts), this method was rejected. For the first analysis, the only completely reliable cat- egory, hand touching the subject's head, face, or neck, was used as a sample of organized movements. The category "other movements" consisted of all the other single-hand move- ments, from little twitches to more or less or- ganized movement~; in connection with postural shifts. Two movements were counted as sepa- rate if them was >5 sec interval in the signal of SCSB (Alihanka 1987). Seven of 54 night recordings were excluded because of their tech- nical inadequacies. Resul t s  The sleep stage analysis was made according to Rechtsehaffen and Kales (1968) and is presented in Table I. There were no differences between Table 1. Sleeping Time and Sleep Stage Percentag,:~ during the Third Night" Patients Controls (.q = 9) (n = I0) p <  Sleeping time (rain) 488.4 + 61,6 REM-Latency (rain) !16,8 + ¶4.0 Wake (%) ! ! .6  + 8,95 NREM-I (%) 12,32 + 10.93 NREM-ll (%) 41,47 + 12.5 NREM-I|I/IV (%) 15,29 + 5.84 REM (%) 19.34 + 5,75 492.2 + 42.0 116.3 + 41.0 3.5 + 4,64 2.57 + 1.83 55.22 + 7.03 16.49 + 4.36 22.20 + 5.63 0.01 NS 0.00i 0.001 NS NS NS p denotes significance of difference between the two groups in t-test. "Mean ± SD, I3rief Reports BIOL PSYCHIATRY ! 93 1992;32: ~ ' | -  194 the patients with and those without the history of occasional drug use. Using the videotapes, 2143 unilateral hand movements were analyzed during sleep, 615 in control group and 682 in PD gro~p. During short periods of nocturnal awakening, the corresponding numbers were 257 and 589. The lateral differences are presented in Table 2. The left/right ratio of 2:1 was the same in REM and NREM sleep as well as short periods of nocturnal wake. There were differ- ences of laterali:,~ation between movement cat- egories, but the difference between controls and the patients in lateralization of movement activ- ity in neutral (prone and supine) positions was insignificant (p < 0.08, Mann-Whitney two- sample rank sum test). Discussion The differences of sleep between PD and normal groups were similar to those of Mailman and Uhde (1989) with regard to normal REM la- tency, and to those of Hauri et ai (1989) with regard to increased movement time, but with no difference in short movements. The laterality results may be somewhat blurred by the absence of handedness data other than the subjective re- port. The diffe ~ence between lateral distribution of clearly or~ anized and other movements is intriguing. "["?e difference might be even more distinct if the category "unorganized" covId be reliably use 1. In our classification, rater bias is highly improbable but the category "other" movements cor~sists partly of organized move- meats. Physiologically, the two movement cate- gories may be different in a fundamental way: organized movements consist of complex se- quences of finger positions that depend primar- ily on the purely contralateral motor system of the precentral gyms, whereas axial movements depend on several other systems, the outflow of which is bilaterally distributed. As the nondom- inant preference is not dependent on the REM/NREM cycle in our study nor in the study of Jovanovic (1971), it may reflect a neural pro- cess different from that indicated by Galliard (1989). There i~ no reason to believe that !land touching face would be a typical nondominant hand function ~hen both hands are free. The findings of Sousa-Poza et al (1979) showed no asymmetry in self-touching during speech, and those of Hampson and Kimura (1984) revealed only slight preference of the left hand in self- touching at the same time the right hand was active in block manipulating. Most recent find- ings confirm the link between hemisphere-spe- cific information processing and simple hand movements (Ashton and McFarland 1991), Dur- ing sleep, the left preferences may be formed, we suppose, by right hemisphere advance in replicating spatial locations (Carnahan and El- liot 1987) and interhemispheric differences ir~ the execution of finger movements, based on different modes of information processing (Bal- foul et al 1991). In light of our findings, it might Table 2. Percentage ot Left Hand Use for Unilateral Hand Movements in Sleep during 3 Nights ° Clearly organized (hand to face) Other unilateral Controls 72.1 + 22.1 (p < 0.04) b 56.5 + 19.6 (NS) b (n -- 9) Patients 64.9 + 18.5 (p < 0.04) 5~.9 + 22.0 (NS) (n = 9) All subjects 6~.2~ + 20.3 (p < 0.002) c 56.2 + 20.3 (NS) c (n = 18) All movements in neutr~ positions 73.5 + 15.1 (p < 0.008) 58.0 + 23.7 (NS) 65.7 + 20.9 (p < 0.006) p (two.tailed) denotes significance of difference between left and right in Wilcoxon-Pran one-sample rank sum test. °Mean - SD (.0 <). Significant difference of laleralization between org~,,zd and other movements: bp < 0.04; ~p < 0.02, Wilcoxon-Pratt test. 194 BIOL PSYCHLATRY Brief Reports 1992;32:191-194 be important to determine the nature of move- ment more closely when using the movement parameters in assessing the motor aspect of sleep in various disorders. Conclusions 1. The results obtained using a new method confirm that the lateral distribution of motor activity during sleep is usually the op~site of that expected on the basis of day-time handedness, with no evident differences be- tween REM and NREM sleep. The bas[~ left to right ratio of 2:1 was the same as in pre- vious EMG studies. 2. The dominance of the left hand is not to be explained by sleeping position. 3. The left dominance in a subgroup of PD pa- tients is not as clear as in normal subjects, which might reflect a deviation in the cere- bral organization or some special feature of the documented ooor quality of their sleep--- with increases in NREM I, awakenings, and complaints about the sleep quality. 4. Self-touching movements to the area of the head and neck are lateralized, but other movements a~  equally distributed, which strongly supports their different neuronal or- igin. The crucial elements in ~he generation of short, unorganized movements with sym- metric distribution may be spinal cord or brainstem disinhibitory processes, whereas the large, organized movements with pyram- idal components reflect cortical activation with possible impac t , of not only motor but also somatosensory and prefrontal cortex. This study was supported by the Gy!lenberg Foundation, Helsinki. We are grateful for the work of Minna Koivikko and of Jouko Haverinen, who did the final visual scoring. References Alihanka J (1987): Basic principles for analyzing and scoring Bio-Matt recordings. Ann Univ Turkuen- sis, Turku. Ashton R, McFarland K (1991): A simple duai-task stu4y of laterality, sex-differences and handed- ness. Cortex 27:105-109. Balfour CA, Clark CR, Geffen GM (1991): Inter- hemispheric differences in the planting and ex- ecution of sequences of skilled finger movements. Neuropsychologia 29:889-905. Blau JN, Wiles CM, Solomon FS (1983): Unilateral somatic symptoms due to hyperventilation BMJ 286:1108. Carnahan H, Elliot D (1987): Pedal asymmetry in ff~e reproduction of spatial locations. Cortex 23:157- 159. Foster FG, Kupfer DJ (1975): Psychomotor activity as a correlate of depression and sl :ep in acute~.y disturbed psychiatric inpatients. Am J Psychiatry 132:928-93 !. Galin D, Diamond R, Braff D (1977): Lateralization of conversion symptoms: More frequent on the left. Am J Psychiat~ 134:578-580. Gaill~d J-M (1989): Brain lateralization during sleep and dreaming. In Home J (ed), Sleep88. Stuttgart, New York: Gustav Fischer Verlag, pp 177-181. Gardner R Jr, Grossman WI (19'16): Normal motor patterns in sleep in man. In Weitzman ED (ed), Advances in Sleep Research 2. New York: Spec- trum Publications, pp 67-107. Hampson E, Kimura D (1984): Hand movement asymmetries during verbal and nonverbal tasks. Can J Psychol 38:102-125. Hauri PJ, Friedman M, Ravaris C w (1989): Sleep in patients with spontaneous panic attacks. Sleep 12:323-337. Jovanovic UJ (I 971): Normal Sleep On Man. Stuttgart: Hippokrates Verlag, pp 99-124. Kmnholm E, Hyypp~i MT (1987): Sleep movements end poor sleep in patients with non-specific so- matic complalnts--ll. Affective disorders and sleep q~ality. J Psychosom Res 31:631-637. Mellman TA, Uhde TW (1989): Eiectroencephalo- graphic sleep in panic .tisorder. Arch Gen Psy- chiatry 46:178-184. Polo O J, Tafti M, Fraga J, Porkka KVK, Dejean Y, Billiard M (1991): Why don't all heavy ~norers have obstructive sleep apnea? Am Rev Respir Dis 143:1288-1293. Rechtschaffen A, Kales AA (1968): A Manual of Standardized Terminology, Techniques and Scor- ing System for Sleep Stages of Hunch Subjects. Washington, DC: National Institute of Public Health, Govermnent Printing Office. Sousa-poza JF, Rohrberg R, Mercure A (1979): Ef- fects of type of information (abstract-concrete) on asymmetry of hand movemetits during speech. Percept Mot Skills 48: I323-1330. 

Laterality of motor activity during normal and disturbed sleep

https://www.utupub.fi/bitstream/10024/155946/1/1-s2.0-000632239290023S-main.pdf

Laterality of motor activity during normal and disturbed sleep

Abstract

Similar works

Full text

Available Versions

UTUPub