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Body movements during night sleep in healthy elderly subjects and their relationships with sleep stages
Brain Research Bulletin 63 (2004) 393–397
Body movements during night sleep in healthy elderly subjects and their relationships with sleep stages Sara Gori a,∗ , Gianluca Ficca b , Fiorenza Giganti b , Ilaria Di Nasso b , Luigi Murri a , Piero Salzarulo b a
Institute of Neurology, Department of Neurosciences, University of Pisa, Via Roma 67, Pisa 56126, Italy b Department of Psychology, University of Florence, Via San Niccolò 93, Florence 50125, Italy Available online 19 May 2004
Abstract In order to enlighten the profile of body movements during sleep at old age, the night sleep of twelve elderly subjects was polygraphically investigated; seven young healthy subjects were the control group. Significantly less body movements during sleep were found in the elderly compared to young subjects, meaning that the decrease in the number of body movements observed from infancy to childhood up to adulthood also continues at later ages. Differently from young adult, whose sleep body movements mainly occur in stage REM, no specific sleep state and/or stage was preferentially associated with the occurrence of body movements in the elderly. These data may point to an age-related modification in the interaction between motor cortex control and subcortical circuits. Furthermore, when body movements occur in elderly individuals, they are significantly more often followed in the next 60 s by a sleep stage change or by a spontaneous behavioural awakening. This might reflect a peculiar inability of elderly subjects to sustain stable states, and could also suggest that body movements may act as a co-factor in a process, comprising other physiological changes, leading to state shifts. © 2004 Elsevier Inc. All rights reserved. Keywords: Body movements; Motility; Sleep; Ageing
1. Introduction Sleep changes across age, from the early epochs of development until old age [3,18]. It has been shown that body movements, an important behavioural aspect of sleep [8], impressively change with age. Modifications already appear very early in development, in particular in the last weeks before term-age [16] and in the first postnatal months [22]. In particular, both the number and the duration of movements decrease in the early postnatal months [22]. In the young adult, beside simple twitches of the distal muscles, there are smaller and larger body movements [25], the latter taking the characteristics of major postural shifts. Accord-
∗ Corresponding author. Tel.: +39-050-992156/992443; fax: +39-050-554808. E-mail address: [email protected] (S. Gori).
0361-9230/$ – see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.brainresbull.2003.12.012
ing to Aaronson et al. [1], there would be about ten of these shifts per night. In the elderly, despite the several physiological changes described during sleep [3,23], the knowledge on the pattern of body movements is still largely incomplete. The first aim of this study has been to evaluate body movements occurring during night sleep in a group of healthy elderly subjects. The frequency and duration of body movements will be compared with the one of younger subjects. The association of body movements to sleep states and their possible connection to states’ transitions is especially remarkable. Muzet et al. [14] suggested that body movements in Stage 2 NREM may delay the transition to slow wave sleep (SWS), whereas their “increase before REM sleep may serve to produce the aroused CNS state necessary for REM sleep”. Also, the alteration of the body movements’ pattern might reflect the deterioration in sleep process [13]. Despite its importance, this topic has been rather neglected
394
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397
so far and very short data exist about the changes with age in the relationship of body movements to sleep states: in both infants [22] and young adults [25], body movements emerge from REM sleep more often than from other stages. To our knowledge, no similar data exist at present with regard to elderly subjects. Thus, a major aim of this study will be to clarify whether in the elderly body movements emerge from different sleep states compared to other age groups and whether they lead more frequently to sleep state changes and possibly to awakening.
2. Method Twelve healthy elderly subjects (M: 10, F: 2, age range: 61–75 years, mean age ± S.D.: 70.5 ± 3.5 years) were recruited on the basis of the following inclusion criteria: (1) active and independent social life; (2) no cognitive impairment evaluated by means of Wechsler Adult Intelligence Scale (WAIS); (3) no signs of serious chronic illness (cardiovascular, osteoarthrosic, urogenitale, endocrine); (4) absence of neurological and/or psychiatric disease; (5) for women, at least 5 years from the beginning of menopause and no hot flashes referred at the clinical interview; (6) negative history for administration of drugs interfering with sleep; (7) no habitual snoring, apnoeas or periodic limb movements (PLM; as confirmed by polysomnography) (8) regular sleep habits (including week-ends) and no complaints for sleep quality or for sleep disturbances. The latter criterion was ascertained by means of sleep log administered for 7 days before the adaptation night. Seven young subjects (M: 4, F: 3, age range: 19–23 years, mean age: 21.4 ± 1.5 years), served as control group. As for the elderly group we assessed the sleep habits before the recording as well as the absence of complaints of sleep disturbances. All participants signed a written informed consent prior to the study. All subjects were non smokers and did not drink alcoholics. The intake of two coffee in a day maximum (in the morning and after lunch) was allowed, as in the habits of subjects in our sample. Before the recording night, subject spent one adaptation night in the sleep laboratory, with complete electrode montage for polysomnography, without recording. On the postadaptation night, the sleep of all subjects was polygraphically recorded, including eight EEG channels (Fp1-C3, C3-T3, T3-O1, C3-O1, Fp2-C4, C4-T4, T4-O2, C4-O2), EOG, submental EMG, EKG, respiration (thoracic, oral and nasal airflow monitoring). Total time in bed allotted was 8 h for that polysomnography was conducted from 11:00 p.m. to 07.00 a.m. of the following day. Bedtime and wake-up time have been chosen according to their consistency with those reported in the habitual sleep diaries filled by the subjects at entrance day. The recordings were scored according to Rechtschaffen and
Kales’ rules [17]. However, slow wave sleep was scored using 40 V as an amplitude criterion as suggested by Webb and Dreblow [24]. The identification of body movements was based, according to Gardner and Grossman’s [8] method, on the recognition of motor artefacts (fast muscle potentials >30 V) in at least half of the EEG and EOG tracings. In our method, body movements were counted when EEG motor artefacts were concomitant with movements separately observed by a blind rater at the video recording. As in Wilde-Frenz and Schulz [25], body movements were distinguished, according to their duration, in Type A movements (shorter than 15 s) and Type B movements (longer than 15 s). Since the number of body movements during sleep also results from the duration of the sleep episode, the rate of their production is given by the ratio: number of body movements/total sleep time in minutes. This rate was calculated for overall body movements and for Types A and B movements separately. Also the occurrence of body movements from each sleep stage was evaluated and the rate of their production is given by the ratio: number of body movements (overall and Types A and B, separately)/duration of each sleep stage in minutes. Mann–Whitney U-test was used to compare the two groups of young and elderly subjects for each dependent variable. Within groups, one-way analysis of variance (ANOVA) was used to address differences in the frequency of occurrence of body movements from each sleep state. Significance level was set at P < 0.05. We also calculated the number of body movements leading, within 60 s, respectively, to a sleep state change or to an awakening. These movements were included in the count of those movements occurring in the sleep state where they started. Due to the different amount of awakenings in the group of young and elderly subjects, we calculated the differences between groups in the probability of waking up after a movement by means of a binomial χ2 -test with π = 1/2.
Table 1 Sleep measures (mean ± S.D.) in elderly and young subjects Elderly Total sleep time (min) Wake after sleep onset (min) Sleep latency (min) Awakenings (min) Stage 1 NREM (min) Stage 1 NREM (%) Stage 2 NREM (min) Stage 2 NREM (%) Slow wave sleep (min) Slow wave sleep (%) REM sleep (min) REM sleep (%) ∗P
< 0.05;
∗∗ P
< 0.01.
354 83 27 4.3 31 8.7 169 47.9 103 29.2 50 14.2
± ± ± ± ± ± ± ± ± ± ± ±
Young 98.4 67 23.6 3.2 13.9 3.2 50.8 4.6 29.0 5.2 25.8 5.0
476 19 8 1.4 16 3.8 237 50.2 102 21.9 121 24.1
± ± ± ± ± ± ± ± ± ± ± ±
P 26.4 22.7 6.4 2.1 11.3 0.9 71.6 7.1 33.4 5.7 16.7 3.5
** ** NS * * * ** NS NS NS ** *
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397
395
Table 2 Frequency of occurrence of body movements, in each sleep stage, for young subjects (n = 7) Stage 1
Stage 2
SWS
REM
F
Least-of-square contrasts REM > SWS∗∗ St.1 > SWS∗∗∗
Total body movements
0.56 ± 0.40
0.32 ± 0.08
0.23 ± 0.07
0.54 ± 0.21
3.55∗
Type A body movements
0.45 ± 0.34
0.28 ± 0.07
0.19 ± 0.08
0.5 ± 0.19
3.46∗
REM > St.2∗ REM > SWS∗∗ St.1 > SWS∗
Type B body movements
0.11 ± 0.08
0.03 ± 0.02
0.03 ± 0.02
0.04 ± 0.04
4.23∗
St.1 > St.2∗∗ St.1 > SWS∗∗ St.1 > REM∗
The frequency is expressed as mean number of movements (±S.D.) per minute spent in that stage. ∗ P < 0.05;
∗∗ P
< 0.01;
∗∗∗ P
< 0.001.
Table 3 Frequency of occurrence of body movements, in each sleep stage, for elderly subjects (n = 12)
Total body movements Type A body movements Type B body movements
Stage 1
Stage 2
SWS
REM
F
P
0.35 ± 0.16 0.37 ± 0.20 0.02 ± 0.02
0.18 ± 0.12 0.20 ± 0.20 0.02 ± 0.02
0.22 ± 0.20 0.21 ± 0.20 0.03 ± 0.03
0.29 ± 0.21 0.27 ± 0.21 0.02 ± 0.05
2.14 1.68 0.04
n.s. n.s. n.s.
The frequency is expressed as mean number of movements (±S.D.) per minute spent in that stage.
3. Results Sleep measures obtained in elderly and young groups are reported in Table 1. Mean number of body movements for each sleep episode was reduced in the elderly compared to young subjects (94.5 versus 172.3). This is accounted for by the reduction of both Type A and Type B movements (86.3 versus 152.0 and 8.1 versus 20.2, respectively). A significant decrease was observed in the elderly also in the rate of total and Type A body movements per sleep minute (total: 0.22 ± 0.12 mov/min versus 0.36 ± 0.08 mov/min; U = 14.0, P = 0.018; Type A: 0.20±0.11 mov/min versus 0.33±0.08 mov/min; U = 13.0, P = 0.014), whereas Type B movements were not modified (0.032 ± 0.04 mov/min versus 0.046 ± 0.02 mov/min; U = 20, n.s.). Tables 2 and 3 show the frequency of occurrence of body movements in each sleep state for the two age groups, re-
40
spectively. In young subjects, movements emerged preferentially from Stage 1 and REM sleep, whether they are the overall or Type A movements, whereas no significant association with stages exists for Type B movements. In the elderly, no significant association was observed between any sleep stage and/or state and the whole number of body movements (although a trend to a higher percentage was found for Stage 1), as well as Type A and Type B movements. In the elderly, a higher percentage of body movements was associated with a sleep stage change in the following 60 s than in young control subjects (total: 20.1% versus 8.6%, P < 0.05; Type A: 18.5% versus 6.8%, P < 0.05; Type B: 36.1% versus 24%, P < 0.001, respectively, in elderly and young subjects; Fig. 1). The percentage of body movements followed by an awakening in the following 60 s is depicted for both age groups: in elderly subjects, this percentage is higher than in young individuals as far as overall and Type A movements are
p<.001
35 30 25 p<.05
p<.05
Elderly Young
% 20 15 10 5 0 Total
Type A
Type B
Fig. 1. Percentage of body movements during sleep followed by a sleep stage change within 60 s in elderly and young subjects.
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concerned (overall: 4.75 versus 1.24, χ2 = 14.46, P = 0.002; Type A: 4.01 versus 0.75, χ2 = 17.7, P = 0.001; Type B: 11.6 versus 4.93, χ2 = 8.9, n.s.).
4. Discussion As also suggested by Gardner and Grossman [8], motor artefacts on the EEG channels turned out to be a “good economic method” to assess global body motility: together with videotape observation, they prevent false positives and show a good intrasubject and “between studies” reliability. In addition, they provide a global measure of movements coming from all different parts of the body (differently from the EMG, which leads on specific districts), which is the actual aim of our study. Night sleep in healthy elderly subjects is characterised by a reduction in the number of body movements in comparison with young control subjects. The trend across age of the frequency of body movements during sleep is one of decrease: the highest frequency is to be observed in the newborn [22], progressively decreasing until the sixth month of life. Later on, children move much more than adults, as already suggested by Garvey [9]; also, DeKoninck et al. [5] showed, by means of all night videotape recordings, that the number of posture changes during sleep decreases from 6 years old to adolescence and to adult age. This trend apparently continues in ageing as well. However, whereas in the young adults the reduction of total body movements is mainly accounted for by the decrease of the gross ones [2], the further decrease in the elderly mainly depends on a diminution of short-lasting movements. In elderly subjects, body movements especially occur in Stage 1 NREM: this essentially replicates what also happens in young adults and comes to little surprise, being Stage 1 an almost indeterminate area between sleep and wake. By contrast, no association between REM sleep and body movements, such as the one occurring in infants [7,21,22] and young adults [25], has been found in old subjects. In elderly subjects, a decrease of the excitability of motoneurons during REM sleep, which at previous ages is clearly higher than in NREM sleep [12], may partly explain this result, as well as the above mentioned age-related decrease in the frequency of movements [15]. The reduction of body motility that elderly subjects especially show in REM sleep could represent one of the phenomena included in a general change of REM-related phasic activity, another peculiar event being for instance the different organization of rapid eye movements [6]. This relative reduction of REM phasic activity could be a first step towards a fading out of the boundaries between sleep states, making these less clearly distinguishable in older subjects [11]. Here we also want to remind that in a sample of elderly subjects our group reported a change in the association with states also of spontaneous awakenings, which do not
emerge significantly more often in REM sleep as they do in young adults [19]. Body movements in the elderly precede a sleep stage change more often than in the young. At this regard, it has to be underscored that sleep stage shifts are a frequent event during the sleep of elderly subjects. An inability to sustain stable states was already described in ageing for long sleep episodes and wakefulness without naps [3,23] and would reflect a peculiar inability of the aged in sustaining prolonged stable physiological activities (a phenomenon described as “functional uncertainty” by Salzarulo et al. [20]). Also the percentage of body movements during sleep, which are followed by spontaneous awakenings, is higher in elderly than in young subjects. This percentage in our study (4.7%) is the same of the one in a previous observation by Kronholm et al. [10]. There is not sufficient evidence to refer to sleep body movements as to events predicting awakening: actually, in elderly individuals, there are also far more awakenings (reflecting a higher degree of fragmentation) not preceded by movements than in young subjects, in agreement with previous findings [23]; however, one might hypothesise that body movements during sleep may sometimes act in the aged as a leading event or, more simply, as a co-factor in a process, probably comprising other changes leading to state shifts. Instability of sleep-related physiological processes is in agreement with data on the increase of arousals as a function of age [4] and with evidences from previous studies of our group on sleep disorganization in elderly subjects [6,20]. In conclusion, despite its high degree of fragmentation and disorganization, elderly individuals’ sleep is less punctuated by body movements than young subjects’. A modified interaction between motor cortex control and subcortical circuits may be invoked to explain this reduction, as also suggested by the changes that the present study shows in the relationship between body movements and sleep states, with particular respect to REM sleep. Further investigation could assess this and other concurrent aspects in determining the age trend of body motility during sleep, such as gender differences, that were not assessed in this study due to the very scarce number of women satisfying the inclusion criteria required for recruitment.
Acknowledgements This research was partially supported by a grant of “Fondazione Cassa di Risparmio, Firenze”. References [1] S.T. Aaronson, S. Rashed, M.P. Biber, J.A. Hobson, Brain state and body position, Arch. Gen. Psychiatry 39 (1982) 330–335. [2] K. Azumi, S. Shirikawa, S.A. Takahashi, Proposal of a new classification for body movements during sleep: variations of body movements through a week, Sleep Res. 6 (1977) 44.
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397 [3] D. Bliwise, Sleep in normal ageing and dementia, Sleep 16 (1993) 40–81. [4] M. Borselli, L. Parrino, A. Smerieri, M.G. Terzano, Effect of age on EEG arousals in normal sleep, Sleep 21 (1998) 351–357. [5] J. DeKoninck, D. Lorrain, P. Gagnon, Sleep positions and position shifts in five age groups: an ontogenetic picture, Sleep 15 (1992) 143–149. [6] G. Ficca, S. Gori, P. Ktonas, C. Quattrini, J. Trammell, P. Salzarulo, The organization of rapid eye movements during Rapid Eye Movement sleep is impaired in the elderly, Neurosci. Lett. 275 (1999) 219–221. [7] F. Findji, P. Catani, D. Paquet, Etude des contractions musculaires au cours du sommeil chez le jeune enfant, Rev. EEG Neurophysiol. Clin. 11 (1981) 51–58. [8] R. Gardner, W.I. Grossman, Normal motor patterns in sleep in man, in: E.D. Weitzmann (Ed.), Advances in Sleep Research, vol. 2, Spectrum Pub., New York, 1976, pp. 67–107. [9] C.R. Garvey, The Activity of Young Children During Sleep, University of Minneapolis Press, Minneapolis, USA, 1939. [10] E. Kronholm, E. Alanem, M.T. Hyppa, Nocturnal motor activity in a community sample, Sleep 16 (1993) 565–571. [11] G.C. Lairy, M. Cor-Mordret, R. Faure, S. Ridjanovic, Etude EEG du sommeil du veillard normal et pathologique, Rev. Neurol. 107 (1962) 188–202. [12] G. Marini, Motor phenomena during sleep, in: M.C. Hepp-Raymond, G. Marini (Eds.), Perspectives of Motor Behaviour and Its Neural Basis, Karger, Basel, 1997, pp. 65–76. [13] A. Muzet, Dynamics of body movements in normal sleep, in: W.P. Koella, F. Obàl, H. Schulz, P. Visser (Eds.), Sleep ’86, Gustav Fischer Verlag, New York, Stuttgart, 1988, pp. 232–234. [14] A. Muzet, P. Naitoh, R.E. Townsend, L.C. Johnson, Body movements during sleep as a predictor of state change, Psychon. Sci. 29 (1972) 7–10. [15] R.W. Oppenheim, Ontogenic adaptations and retrogressive processes in the development of the nervous system and behaviour: a neu-
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23] [24] [25]
397
roembryological perspective, in: K.J. Connolly, H.F.R. Prechtl (Eds.), Maturation and Development, W. Henemann Medical Books, London, 1981, pp. 73–109. P. Peirano, L. Curzi-Dascalova, G. Korn, Influence of sleep state and age on body motility in normal, premature and full term neonates, Neuropediatrics 17 (1986) 186–190. A. Rechtschaffen, A. Kales, A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects, Public Health Service, US, Government Printing Office, Washington, DC, 1968. P. Salzarulo, I. Fagioli, Changes of sleep states and physiological activities across the first year of life, in: A. Kalverboer, M.L. Genta, B. Hopkins (Eds.), Current Issues in Developmental Psychology. Biopsychological Perspectives, Kluwer, Dordrecht, 1999, pp. 53–74. P. Salzarulo, I. Fagioli, P. Lombardo, S. Gori, C. Gneri, R. Chiaramonti, L. Murri, Sleep stages preceding spontaneous awakenings in the elderly, Sleep Res. Online 2 (1999) 73–77. P. Salzarulo, G. Formicola, P. Lombardo, S. Gori, L. Rossi, L. Murri, C. Cipolli, Functional uncertainty, ageing and memory processes during sleep, Acta Neurol. Belg. 97 (1997) 118–122. M.F. Vecchierini-Blineau, B. Nogues, S. Louvet, Etude des mouvements corporels au cours du someil chez le nourrisson: comparaison entre nourrissons témoins et nourrissons issus d’une fratrie de mort subite inexpliquée du nourrisson, Rev. EEG Neurophysiol. Clin. 16 (1986) 21–27. M.F. Vecchierini-Blineau, B. Nogues, S. Louvet, O. Desfontaines, Maturation de la motilité généralisée, spontanée au cours de sommeil, de la naissance à terme à l’ˆage de 6 mois, Neurophysiol. Clin. 24 (1994) 141–154. W.B. Webb, The measurement and characteristics of sleep in older persons, Neurobiol. Ageing 3 (1982) 311–319. W.B. Webb, L.M. Dreblow, A modified method for scoring slow wave sleep of older subjects, Sleep 5 (1982) 195–199. J. Wilde-Frenz, H. Schulz, Rate and distribution of body movements during sleep in humans, Percept. Mot. Skills 56 (1983) 275–283.
Body movements during night sleep in healthy elderly subjects and their relationships with sleep stages Sara Gori a,∗ , Gianluca Ficca b , Fiorenza Giganti b , Ilaria Di Nasso b , Luigi Murri a , Piero Salzarulo b a
Institute of Neurology, Department of Neurosciences, University of Pisa, Via Roma 67, Pisa 56126, Italy b Department of Psychology, University of Florence, Via San Niccolò 93, Florence 50125, Italy Available online 19 May 2004
Abstract In order to enlighten the profile of body movements during sleep at old age, the night sleep of twelve elderly subjects was polygraphically investigated; seven young healthy subjects were the control group. Significantly less body movements during sleep were found in the elderly compared to young subjects, meaning that the decrease in the number of body movements observed from infancy to childhood up to adulthood also continues at later ages. Differently from young adult, whose sleep body movements mainly occur in stage REM, no specific sleep state and/or stage was preferentially associated with the occurrence of body movements in the elderly. These data may point to an age-related modification in the interaction between motor cortex control and subcortical circuits. Furthermore, when body movements occur in elderly individuals, they are significantly more often followed in the next 60 s by a sleep stage change or by a spontaneous behavioural awakening. This might reflect a peculiar inability of elderly subjects to sustain stable states, and could also suggest that body movements may act as a co-factor in a process, comprising other physiological changes, leading to state shifts. © 2004 Elsevier Inc. All rights reserved. Keywords: Body movements; Motility; Sleep; Ageing
1. Introduction Sleep changes across age, from the early epochs of development until old age [3,18]. It has been shown that body movements, an important behavioural aspect of sleep [8], impressively change with age. Modifications already appear very early in development, in particular in the last weeks before term-age [16] and in the first postnatal months [22]. In particular, both the number and the duration of movements decrease in the early postnatal months [22]. In the young adult, beside simple twitches of the distal muscles, there are smaller and larger body movements [25], the latter taking the characteristics of major postural shifts. Accord-
∗ Corresponding author. Tel.: +39-050-992156/992443; fax: +39-050-554808. E-mail address: [email protected] (S. Gori).
0361-9230/$ – see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.brainresbull.2003.12.012
ing to Aaronson et al. [1], there would be about ten of these shifts per night. In the elderly, despite the several physiological changes described during sleep [3,23], the knowledge on the pattern of body movements is still largely incomplete. The first aim of this study has been to evaluate body movements occurring during night sleep in a group of healthy elderly subjects. The frequency and duration of body movements will be compared with the one of younger subjects. The association of body movements to sleep states and their possible connection to states’ transitions is especially remarkable. Muzet et al. [14] suggested that body movements in Stage 2 NREM may delay the transition to slow wave sleep (SWS), whereas their “increase before REM sleep may serve to produce the aroused CNS state necessary for REM sleep”. Also, the alteration of the body movements’ pattern might reflect the deterioration in sleep process [13]. Despite its importance, this topic has been rather neglected
394
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397
so far and very short data exist about the changes with age in the relationship of body movements to sleep states: in both infants [22] and young adults [25], body movements emerge from REM sleep more often than from other stages. To our knowledge, no similar data exist at present with regard to elderly subjects. Thus, a major aim of this study will be to clarify whether in the elderly body movements emerge from different sleep states compared to other age groups and whether they lead more frequently to sleep state changes and possibly to awakening.
2. Method Twelve healthy elderly subjects (M: 10, F: 2, age range: 61–75 years, mean age ± S.D.: 70.5 ± 3.5 years) were recruited on the basis of the following inclusion criteria: (1) active and independent social life; (2) no cognitive impairment evaluated by means of Wechsler Adult Intelligence Scale (WAIS); (3) no signs of serious chronic illness (cardiovascular, osteoarthrosic, urogenitale, endocrine); (4) absence of neurological and/or psychiatric disease; (5) for women, at least 5 years from the beginning of menopause and no hot flashes referred at the clinical interview; (6) negative history for administration of drugs interfering with sleep; (7) no habitual snoring, apnoeas or periodic limb movements (PLM; as confirmed by polysomnography) (8) regular sleep habits (including week-ends) and no complaints for sleep quality or for sleep disturbances. The latter criterion was ascertained by means of sleep log administered for 7 days before the adaptation night. Seven young subjects (M: 4, F: 3, age range: 19–23 years, mean age: 21.4 ± 1.5 years), served as control group. As for the elderly group we assessed the sleep habits before the recording as well as the absence of complaints of sleep disturbances. All participants signed a written informed consent prior to the study. All subjects were non smokers and did not drink alcoholics. The intake of two coffee in a day maximum (in the morning and after lunch) was allowed, as in the habits of subjects in our sample. Before the recording night, subject spent one adaptation night in the sleep laboratory, with complete electrode montage for polysomnography, without recording. On the postadaptation night, the sleep of all subjects was polygraphically recorded, including eight EEG channels (Fp1-C3, C3-T3, T3-O1, C3-O1, Fp2-C4, C4-T4, T4-O2, C4-O2), EOG, submental EMG, EKG, respiration (thoracic, oral and nasal airflow monitoring). Total time in bed allotted was 8 h for that polysomnography was conducted from 11:00 p.m. to 07.00 a.m. of the following day. Bedtime and wake-up time have been chosen according to their consistency with those reported in the habitual sleep diaries filled by the subjects at entrance day. The recordings were scored according to Rechtschaffen and
Kales’ rules [17]. However, slow wave sleep was scored using 40 V as an amplitude criterion as suggested by Webb and Dreblow [24]. The identification of body movements was based, according to Gardner and Grossman’s [8] method, on the recognition of motor artefacts (fast muscle potentials >30 V) in at least half of the EEG and EOG tracings. In our method, body movements were counted when EEG motor artefacts were concomitant with movements separately observed by a blind rater at the video recording. As in Wilde-Frenz and Schulz [25], body movements were distinguished, according to their duration, in Type A movements (shorter than 15 s) and Type B movements (longer than 15 s). Since the number of body movements during sleep also results from the duration of the sleep episode, the rate of their production is given by the ratio: number of body movements/total sleep time in minutes. This rate was calculated for overall body movements and for Types A and B movements separately. Also the occurrence of body movements from each sleep stage was evaluated and the rate of their production is given by the ratio: number of body movements (overall and Types A and B, separately)/duration of each sleep stage in minutes. Mann–Whitney U-test was used to compare the two groups of young and elderly subjects for each dependent variable. Within groups, one-way analysis of variance (ANOVA) was used to address differences in the frequency of occurrence of body movements from each sleep state. Significance level was set at P < 0.05. We also calculated the number of body movements leading, within 60 s, respectively, to a sleep state change or to an awakening. These movements were included in the count of those movements occurring in the sleep state where they started. Due to the different amount of awakenings in the group of young and elderly subjects, we calculated the differences between groups in the probability of waking up after a movement by means of a binomial χ2 -test with π = 1/2.
Table 1 Sleep measures (mean ± S.D.) in elderly and young subjects Elderly Total sleep time (min) Wake after sleep onset (min) Sleep latency (min) Awakenings (min) Stage 1 NREM (min) Stage 1 NREM (%) Stage 2 NREM (min) Stage 2 NREM (%) Slow wave sleep (min) Slow wave sleep (%) REM sleep (min) REM sleep (%) ∗P
< 0.05;
∗∗ P
< 0.01.
354 83 27 4.3 31 8.7 169 47.9 103 29.2 50 14.2
± ± ± ± ± ± ± ± ± ± ± ±
Young 98.4 67 23.6 3.2 13.9 3.2 50.8 4.6 29.0 5.2 25.8 5.0
476 19 8 1.4 16 3.8 237 50.2 102 21.9 121 24.1
± ± ± ± ± ± ± ± ± ± ± ±
P 26.4 22.7 6.4 2.1 11.3 0.9 71.6 7.1 33.4 5.7 16.7 3.5
** ** NS * * * ** NS NS NS ** *
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397
395
Table 2 Frequency of occurrence of body movements, in each sleep stage, for young subjects (n = 7) Stage 1
Stage 2
SWS
REM
F
Least-of-square contrasts REM > SWS∗∗ St.1 > SWS∗∗∗
Total body movements
0.56 ± 0.40
0.32 ± 0.08
0.23 ± 0.07
0.54 ± 0.21
3.55∗
Type A body movements
0.45 ± 0.34
0.28 ± 0.07
0.19 ± 0.08
0.5 ± 0.19
3.46∗
REM > St.2∗ REM > SWS∗∗ St.1 > SWS∗
Type B body movements
0.11 ± 0.08
0.03 ± 0.02
0.03 ± 0.02
0.04 ± 0.04
4.23∗
St.1 > St.2∗∗ St.1 > SWS∗∗ St.1 > REM∗
The frequency is expressed as mean number of movements (±S.D.) per minute spent in that stage. ∗ P < 0.05;
∗∗ P
< 0.01;
∗∗∗ P
< 0.001.
Table 3 Frequency of occurrence of body movements, in each sleep stage, for elderly subjects (n = 12)
Total body movements Type A body movements Type B body movements
Stage 1
Stage 2
SWS
REM
F
P
0.35 ± 0.16 0.37 ± 0.20 0.02 ± 0.02
0.18 ± 0.12 0.20 ± 0.20 0.02 ± 0.02
0.22 ± 0.20 0.21 ± 0.20 0.03 ± 0.03
0.29 ± 0.21 0.27 ± 0.21 0.02 ± 0.05
2.14 1.68 0.04
n.s. n.s. n.s.
The frequency is expressed as mean number of movements (±S.D.) per minute spent in that stage.
3. Results Sleep measures obtained in elderly and young groups are reported in Table 1. Mean number of body movements for each sleep episode was reduced in the elderly compared to young subjects (94.5 versus 172.3). This is accounted for by the reduction of both Type A and Type B movements (86.3 versus 152.0 and 8.1 versus 20.2, respectively). A significant decrease was observed in the elderly also in the rate of total and Type A body movements per sleep minute (total: 0.22 ± 0.12 mov/min versus 0.36 ± 0.08 mov/min; U = 14.0, P = 0.018; Type A: 0.20±0.11 mov/min versus 0.33±0.08 mov/min; U = 13.0, P = 0.014), whereas Type B movements were not modified (0.032 ± 0.04 mov/min versus 0.046 ± 0.02 mov/min; U = 20, n.s.). Tables 2 and 3 show the frequency of occurrence of body movements in each sleep state for the two age groups, re-
40
spectively. In young subjects, movements emerged preferentially from Stage 1 and REM sleep, whether they are the overall or Type A movements, whereas no significant association with stages exists for Type B movements. In the elderly, no significant association was observed between any sleep stage and/or state and the whole number of body movements (although a trend to a higher percentage was found for Stage 1), as well as Type A and Type B movements. In the elderly, a higher percentage of body movements was associated with a sleep stage change in the following 60 s than in young control subjects (total: 20.1% versus 8.6%, P < 0.05; Type A: 18.5% versus 6.8%, P < 0.05; Type B: 36.1% versus 24%, P < 0.001, respectively, in elderly and young subjects; Fig. 1). The percentage of body movements followed by an awakening in the following 60 s is depicted for both age groups: in elderly subjects, this percentage is higher than in young individuals as far as overall and Type A movements are
p<.001
35 30 25 p<.05
p<.05
Elderly Young
% 20 15 10 5 0 Total
Type A
Type B
Fig. 1. Percentage of body movements during sleep followed by a sleep stage change within 60 s in elderly and young subjects.
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concerned (overall: 4.75 versus 1.24, χ2 = 14.46, P = 0.002; Type A: 4.01 versus 0.75, χ2 = 17.7, P = 0.001; Type B: 11.6 versus 4.93, χ2 = 8.9, n.s.).
4. Discussion As also suggested by Gardner and Grossman [8], motor artefacts on the EEG channels turned out to be a “good economic method” to assess global body motility: together with videotape observation, they prevent false positives and show a good intrasubject and “between studies” reliability. In addition, they provide a global measure of movements coming from all different parts of the body (differently from the EMG, which leads on specific districts), which is the actual aim of our study. Night sleep in healthy elderly subjects is characterised by a reduction in the number of body movements in comparison with young control subjects. The trend across age of the frequency of body movements during sleep is one of decrease: the highest frequency is to be observed in the newborn [22], progressively decreasing until the sixth month of life. Later on, children move much more than adults, as already suggested by Garvey [9]; also, DeKoninck et al. [5] showed, by means of all night videotape recordings, that the number of posture changes during sleep decreases from 6 years old to adolescence and to adult age. This trend apparently continues in ageing as well. However, whereas in the young adults the reduction of total body movements is mainly accounted for by the decrease of the gross ones [2], the further decrease in the elderly mainly depends on a diminution of short-lasting movements. In elderly subjects, body movements especially occur in Stage 1 NREM: this essentially replicates what also happens in young adults and comes to little surprise, being Stage 1 an almost indeterminate area between sleep and wake. By contrast, no association between REM sleep and body movements, such as the one occurring in infants [7,21,22] and young adults [25], has been found in old subjects. In elderly subjects, a decrease of the excitability of motoneurons during REM sleep, which at previous ages is clearly higher than in NREM sleep [12], may partly explain this result, as well as the above mentioned age-related decrease in the frequency of movements [15]. The reduction of body motility that elderly subjects especially show in REM sleep could represent one of the phenomena included in a general change of REM-related phasic activity, another peculiar event being for instance the different organization of rapid eye movements [6]. This relative reduction of REM phasic activity could be a first step towards a fading out of the boundaries between sleep states, making these less clearly distinguishable in older subjects [11]. Here we also want to remind that in a sample of elderly subjects our group reported a change in the association with states also of spontaneous awakenings, which do not
emerge significantly more often in REM sleep as they do in young adults [19]. Body movements in the elderly precede a sleep stage change more often than in the young. At this regard, it has to be underscored that sleep stage shifts are a frequent event during the sleep of elderly subjects. An inability to sustain stable states was already described in ageing for long sleep episodes and wakefulness without naps [3,23] and would reflect a peculiar inability of the aged in sustaining prolonged stable physiological activities (a phenomenon described as “functional uncertainty” by Salzarulo et al. [20]). Also the percentage of body movements during sleep, which are followed by spontaneous awakenings, is higher in elderly than in young subjects. This percentage in our study (4.7%) is the same of the one in a previous observation by Kronholm et al. [10]. There is not sufficient evidence to refer to sleep body movements as to events predicting awakening: actually, in elderly individuals, there are also far more awakenings (reflecting a higher degree of fragmentation) not preceded by movements than in young subjects, in agreement with previous findings [23]; however, one might hypothesise that body movements during sleep may sometimes act in the aged as a leading event or, more simply, as a co-factor in a process, probably comprising other changes leading to state shifts. Instability of sleep-related physiological processes is in agreement with data on the increase of arousals as a function of age [4] and with evidences from previous studies of our group on sleep disorganization in elderly subjects [6,20]. In conclusion, despite its high degree of fragmentation and disorganization, elderly individuals’ sleep is less punctuated by body movements than young subjects’. A modified interaction between motor cortex control and subcortical circuits may be invoked to explain this reduction, as also suggested by the changes that the present study shows in the relationship between body movements and sleep states, with particular respect to REM sleep. Further investigation could assess this and other concurrent aspects in determining the age trend of body motility during sleep, such as gender differences, that were not assessed in this study due to the very scarce number of women satisfying the inclusion criteria required for recruitment.
Acknowledgements This research was partially supported by a grant of “Fondazione Cassa di Risparmio, Firenze”. References [1] S.T. Aaronson, S. Rashed, M.P. Biber, J.A. Hobson, Brain state and body position, Arch. Gen. Psychiatry 39 (1982) 330–335. [2] K. Azumi, S. Shirikawa, S.A. Takahashi, Proposal of a new classification for body movements during sleep: variations of body movements through a week, Sleep Res. 6 (1977) 44.
S. Gori et al. / Brain Research Bulletin 63 (2004) 393–397 [3] D. Bliwise, Sleep in normal ageing and dementia, Sleep 16 (1993) 40–81. [4] M. Borselli, L. Parrino, A. Smerieri, M.G. Terzano, Effect of age on EEG arousals in normal sleep, Sleep 21 (1998) 351–357. [5] J. DeKoninck, D. Lorrain, P. Gagnon, Sleep positions and position shifts in five age groups: an ontogenetic picture, Sleep 15 (1992) 143–149. [6] G. Ficca, S. Gori, P. Ktonas, C. Quattrini, J. Trammell, P. Salzarulo, The organization of rapid eye movements during Rapid Eye Movement sleep is impaired in the elderly, Neurosci. Lett. 275 (1999) 219–221. [7] F. Findji, P. Catani, D. Paquet, Etude des contractions musculaires au cours du sommeil chez le jeune enfant, Rev. EEG Neurophysiol. Clin. 11 (1981) 51–58. [8] R. Gardner, W.I. Grossman, Normal motor patterns in sleep in man, in: E.D. Weitzmann (Ed.), Advances in Sleep Research, vol. 2, Spectrum Pub., New York, 1976, pp. 67–107. [9] C.R. Garvey, The Activity of Young Children During Sleep, University of Minneapolis Press, Minneapolis, USA, 1939. [10] E. Kronholm, E. Alanem, M.T. Hyppa, Nocturnal motor activity in a community sample, Sleep 16 (1993) 565–571. [11] G.C. Lairy, M. Cor-Mordret, R. Faure, S. Ridjanovic, Etude EEG du sommeil du veillard normal et pathologique, Rev. Neurol. 107 (1962) 188–202. [12] G. Marini, Motor phenomena during sleep, in: M.C. Hepp-Raymond, G. Marini (Eds.), Perspectives of Motor Behaviour and Its Neural Basis, Karger, Basel, 1997, pp. 65–76. [13] A. Muzet, Dynamics of body movements in normal sleep, in: W.P. Koella, F. Obàl, H. Schulz, P. Visser (Eds.), Sleep ’86, Gustav Fischer Verlag, New York, Stuttgart, 1988, pp. 232–234. [14] A. Muzet, P. Naitoh, R.E. Townsend, L.C. Johnson, Body movements during sleep as a predictor of state change, Psychon. Sci. 29 (1972) 7–10. [15] R.W. Oppenheim, Ontogenic adaptations and retrogressive processes in the development of the nervous system and behaviour: a neu-
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23] [24] [25]
397
roembryological perspective, in: K.J. Connolly, H.F.R. Prechtl (Eds.), Maturation and Development, W. Henemann Medical Books, London, 1981, pp. 73–109. P. Peirano, L. Curzi-Dascalova, G. Korn, Influence of sleep state and age on body motility in normal, premature and full term neonates, Neuropediatrics 17 (1986) 186–190. A. Rechtschaffen, A. Kales, A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects, Public Health Service, US, Government Printing Office, Washington, DC, 1968. P. Salzarulo, I. Fagioli, Changes of sleep states and physiological activities across the first year of life, in: A. Kalverboer, M.L. Genta, B. Hopkins (Eds.), Current Issues in Developmental Psychology. Biopsychological Perspectives, Kluwer, Dordrecht, 1999, pp. 53–74. P. Salzarulo, I. Fagioli, P. Lombardo, S. Gori, C. Gneri, R. Chiaramonti, L. Murri, Sleep stages preceding spontaneous awakenings in the elderly, Sleep Res. Online 2 (1999) 73–77. P. Salzarulo, G. Formicola, P. Lombardo, S. Gori, L. Rossi, L. Murri, C. Cipolli, Functional uncertainty, ageing and memory processes during sleep, Acta Neurol. Belg. 97 (1997) 118–122. M.F. Vecchierini-Blineau, B. Nogues, S. Louvet, Etude des mouvements corporels au cours du someil chez le nourrisson: comparaison entre nourrissons témoins et nourrissons issus d’une fratrie de mort subite inexpliquée du nourrisson, Rev. EEG Neurophysiol. Clin. 16 (1986) 21–27. M.F. Vecchierini-Blineau, B. Nogues, S. Louvet, O. Desfontaines, Maturation de la motilité généralisée, spontanée au cours de sommeil, de la naissance à terme à l’ˆage de 6 mois, Neurophysiol. Clin. 24 (1994) 141–154. W.B. Webb, The measurement and characteristics of sleep in older persons, Neurobiol. Ageing 3 (1982) 311–319. W.B. Webb, L.M. Dreblow, A modified method for scoring slow wave sleep of older subjects, Sleep 5 (1982) 195–199. J. Wilde-Frenz, H. Schulz, Rate and distribution of body movements during sleep in humans, Percept. Mot. Skills 56 (1983) 275–283.