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The role of arousals during sleep stages and cycles in human sleep development and quality. The study analyzes conventional sleep parameters, arousal indices, and their correlation with the Pittsburgh Sleep Quality Index (PSQI). The document also explores the impact of sleep fragmentation on sleep restorative function and the relationship between sleep stages and arousals.
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Zakevicius Martynas^1 , Liesiene Vanda^2 , Griksiene Ramune^1 , Masaitiene Raminta^3 , Ruksenas Osvaldas^1 Study carried out at Department of Neurobiology and Biophysics, Faculty of Natural Sciences, Vilnius University, Vilnius, Lithuania. (^1) Department of Neurobiology and Biophysics, Faculty of Natural Sciences, Vilnius University, Vilnius, Lithuania. (^2) Institute of Neuromedicine, Kaunas, Lithuania. (^3) Sleep disorders laboratory, Vilnius Sapiegos Hospital, Vilnius, Lithuania. Corresponding author: Martynas Zakevicius. Department of Neurobiology and Biophysics, Vilnius Universit. M.K. Ciurlionio st. 21/27, 03101 Vilnius, Lithuania. Phone: +370 605 84 607. Fax: +370 5 239 8216. E-mail: martis54@gmail.com Received: February 26, 2013; Accepted: August 26, 2013.
Objectives: The sense of rest after sleep and its relation to various sleep parameters is still a debatable issue. The purpose of the present study was to analyse sleep fragmentation by scoring various arousals (microarousals (MA), vegetative (VA) and behavioural (BA) arousals) in all sleep stages and to evaluate their relation with subjective sleep quality without paying attention to the type of insomnia. Methods: The overnight sleep cycles of 60 subjects were analyzed according to their stage composition and arousals. Arousal indices (AI) were calculated for all types of arousals in all sleep stages and sleep cycles. The sleep quality was quantified using the Pittsburgh sleep quality index (PSQI). Results: AI differences between sleep cycles were not statistically significant. MAI value in total sleep time (TST) - 5.8 ± SD 4.1 - was the highest among all the three arousal types. Differences between AI in most sleep stages were statistically significant for all types of arousals. This suggests that human sleep development within a single sleep cycle is more important for the sleep quality than the changes between different sleep cycles. The highest AI scores for the three types of arousals were found in NREM stage 2. The strongest and significant correlation was between PSQI and MAI (r = 0.42; p = 0 .001). Conclusion: The density of microarousals is impor- tant for the subjective sleep quality. The highest values of MAI and other arousal types are found in NREM stage 2. The importance of this stage might be higher than thought before and especially in initial sleep cycles. Keywords: sleep, sleep arousals disorders, sleep stages. RESUMO Objetivos: O sentido de descanso após o sono e sua relação com vários parâmetros do sono ainda é uma questão discutível. O obje- tivo do presente estudo foi analisar a fragmentação do sono, mar- cando vários despertares (microdespertares (MA), vegetativas (VA) e comportamentais (BA) despertares) em todas as fases do sono e avaliar sua relação com a qualidade subjetiva do sono, sem prestar atenção ao tipo de insônia. Métodos: Os ciclos de sono durante a noite de 60 indivíduos foram analisados de acordo com a sua composição palco e despertares. Índices de excitação (AI) foram calculados para todos os tipos de despertares em todas as fases do sono e os ciclos do sono. A qualidade do sono foi quantifica-
The overnight course of sleep is not a simple linear process, and it exhibits a very complex behavior which involves various areas of the central nervous system at different levels and at different times(1). The daily shifts from the wake state to NREM and REM sleep are under the control of interconnected processes, including the circadian timing of sleep onset, the homeostatic balance between wakefulness and sleep and the ultradian interaction between NREM and REM sleep(2). More recently, and especially to explain the clinical consequences of sleep disorders, the three processes of sleep regulation - circadian, homeostatic and ultradian - have been integrated by the definition of the arousal system(3). Arousals are transient episodes of cerebral activation during sleep which involves massively the cortex regulated by the interplay between cortical and subcortical neurons(3,4). Most authors consider arousals as a transient cortical activation in response to sleep disruptive events(5-7), but there are other studies indicating that Descritores: fases do sono, sono, transtornos do despertar do sono. da através do índice de qualidade do sono de Pittsburgh (PSQI). Resultados: Diferenças entre AI ciclos de sono não foram estatis- ticamente significativas. MAI valor no tempo total de sono (TST)
(^92) Arousals and Sleep Quality arousals punctuate both REM and NREM sleep even in the absence of detectable disturbing stimuli(8,9). On the one hand, there are debates still going on about the nature and role of arousals in sleep, and on the other hand, there is a question about their role for the sleeper him/herself - how his/her sleep quality is affected by them. There are various stud- ies trying to evaluate a person’s sense of rest after the sleep in the morning, but researchers still disagree about what determines the sense of rest after the sleep(10). There are findings which showed that the subjective satisfaction after the sleep is not dependent on the overall sleep length(11). It was assumed that the amount of delta sleep is very important in sleep structure, but it wasn’t ex- actly confirmed and even people with sufficient amounts of deep sleep might feel unrested in the morning(5). A lot of attention is recently paid to the sleep integrity and the role of sleep fragmen- tation, which is characteristic of primary insomnia and could have an effect on the sleep’s restorative function(12,13). The aim of the present study was to analyze sleep fragmentation by scoring different type arousals in all sleep stages and cycles and to evaluate their relationship with the subjective sense of rest after the sleep without paying attention to the type of insomnia.
The data analyzed in this study were collected from the all night polysomnographic (PSG) recordings of 60 subjects ( men and 30 women) aged between 36 and 55 years (mean 46 ± SD 5.6 years). Subjects were recruited from clinical patients of the Sleep disorders laboratory at Vilnius Sapiegos hospital in Vilnius. All subjects were diagnosed with various sleep disorders. The only exclusion criteria were sleep apneas and heavy snoring problems. They had all night PSG study performed in the sleep disorders laboratory and woke up in the morning at their usual time. Before the study, patients had consultations with the doctor, filled out necessary questionnaires and provided written informed consents. All clinical experiments conformed to the principles outlined by the Declaration of Helsinki.
A monopolar derivation (C3-A2 or C4-A1) was used to score sleep stages(14)^ and arousals. Arousals were scored and arousal indices (AI) (the number of arousals per hour of sleep) were calculated in three major groups to represent different levels of cortical and somatovegetative activations:
The Pittsburgh Sleep Quality Index (PSQI)(17)^ was developed to measure sleep quality during the previous month and to discriminate between good and poor sleepers. The PSQI has been used to measure sleep quality among truck drivers(18), to test the effects of a drug on sleep quality in a randomized placebo controlled trial(19)^ and others. Sleep quality is a complex phenomenon that involves several dimensions, each of which is covered by the PSQI. The covered domains include Subjective Sleep Quality, Sleep Latency, Sleep Duration, Habitual Sleep Efficiency, Sleep Disturbances, Use of Sleep Medications, and Daytime Dysfunction. The PSQI is designed to assess sleep quality during the past month and con- tains 19 self-rated questions and 5 questions rated by a bed part- ner or roommate (only the self-rated items are used in scoring the scale). Seven component scores that correspond to the domains listed previously are calculated and summed into a global score(17). A score of 5 and more indicates poor sleep quality; the higher the score, the worse the sleep quality. Component scores range from 0 to 3 and global scores range from 0 to 21.
All patients who took part in the study were patients of the Sleep disorders laboratory in Vilnius Sapiegos hospital. As part of their standard clinical assessment they completed the PSQI at their initial patient consultation and a clinical history was taken. An overnight sleep study was then performed using the electrophysiological recording equipment (SleepLab Applications from VIASYS®^ Respiratory Care Inc., Viasys Healthcare GmbH, Hoechberg, Germany) to measure 4 EEG leads (C3, C4, P3, P4 referenced to linked ears), an electrooculogram (EOG), an electromyogram (EMG), and an electrocardiogram (ECG). Also arterial oxygen saturation (SaO 2 ) was determined, respiration was monitored with thermistors and thoracic movements, and tibialis electromyographic activ- ity was recorded using surface electrodes placed on the right and left legs. The sleep laboratory was equipped with video and sound recording devices for additional monitoring of body movements and sounds. All equipment was time synchronized. Subjects went to bed at their usual time and were asked to refrain from drinking beverages containing caffeine or alcohol in the previous afternoon and evening hours. In the morning they also awakened at their usual time. Sleep stages were visually scored according to standard criteria(14)^ using 30-second epochs, with the investigator blind to subject and experimental conditions. Standard sleep parameters were computed over the complete sleep time period, and all recordings were analyzed for sleep staging and arousal scoring with the Matrix Sleep Analysis SleepLab®^ for Windows (version 1.70.0.3) software package.
(^94) Arousals and Sleep Quality Table 1. Stage duration in sleep cycles. I cycle II cycle III cycle IV cycle V cycle p F Significantly differing sleep cycles Number of subjects 44 44 41 40 24 TST (min) 86.4 ± 21.8 92.3 ± 19.6 94.8 ± 30.0 92.6 ± 18.2 83.5 ± 24.3 n. s. WASO (min) 6.4 ± 8.1 4.0 ± 6.7 6.9 ± 9.6 4.6 ± 8.7 4.9 ± 8.2 n. s. N1 (min) 11.5 ± 8.6 6.6 ± 7.2 9.5 ± 13.5 9.1 ± 9.1 12.5 ± 2.3 n. s. N2 (min) 23.0 ± 11.4 29.7 ± 12.9 36.8 ± 12.3 37.1 ± 13.2 34.6 ± 14.3 < 0.001 1.342 3 > 1; 4 > 1; 5 > 1 N3 (min) 23.9 ± 12.7 23.9 ± 12.7 18.9 ± 15.8 11.3 ± 9.7 4.5 ± 6.1 < 0.001 1.717 1 > 4; 1 > 5; 2 > 4; 2 > 5; 3 > 5 N4 (min) 12.8 ± 12.5 10.8 ± 11.1 4.1 ± 6.9 3.8 ± 7.6 1.4 ± 4.9 < 0.05 6.439 1 > 5; NREM (min) 71.1 ± 16.5 70.9 ± 17.2 69.3 ± 21.3 61.3 ± 15.4 53.0 ± 16.4 n. s. REM (min) 8.8 ± 8.0 17.4 ± 12.6 18.7 ± 13.4 26.6 ± 15.0 25.6 ± 14.6 < 0.05 3.293 3 > 1; 4 > 1; 5 > 1; TST: Total sleep time; WASO: Wake after sleep onset; N1, N2, N3, N4: Stages 1, 2, 3, 4; NREM: Non-rapid eye movement sleep; REM: Rapid eye movement sleep; p : Significance of inter cycle differences; F: F-ratio variance; Average ± SD. Figure 1. Average proportions of light sleep (LS), deep sleep (DS) and REM sleep in different sleep cycles; N: Number of subjects. Table 2. Arousal indices in sleep cycles. I cycle II cycle III cycle IV cycle V cycle Number of subjects 46 45 42 40 24 BAI 4.7 ± 4.1 5.3 ± 4.4 3.9 ± 2.7 3.7 ± 3.0 4.2 ± 3. MAI 4.4 ± 4.0 5.2 ± 5.5 5.1 ± 4.2 4.1 ± 3.3 6.9 ± 5. VAI 1.6 ± 1.7 3.2 ± 3.3 2.6 ± 2.7 2.9 ± 2.8 3.3 ± 3. BAI: Behavioural arousal index; MAI: Microarousal index; VAI: Vegetative arousal index; Average ± SD. Correlations between the amount of light sleep and deep sleep in sleep cycles with PSQI were not significant. This relation in case of deep sleep from negative (r = -0.20) becomes neutral (r = 0.04) going from the first to the fifth sleep cycle and in case of light sleep - from positive (r = 0.23) to more neutral (r = 0.12). The correlation between the amount of REM sleep and PSQI values varies a lot from one sleep cycle to another over the night (Figure 3). The correlation between different types of AIs and PSQIs changes during the night. MAI correlation rises during the night while BAI and VAI decrease (Figure 4). Statistically significant correlation with PSQI showed only BAI (r = -0.34; p = 0.02) and VAI (r = -0.33; p = 0.03) in the fifth sleep cycle. AI’s dynamics during the night is closely related to the duration of sleep stages in each sleep cycle.
The present study was undertaken to analyse sleep structure and fragmentation in terms of arousals (behavioural, micro and vegetative) and their distribution during the night and to evaluate if there is any relation with the subjective sense of rest after the sleep without paying attention to the type of insomnia. Stage-dependent EEG modifications, the cyclic alternation between NREM and REM sleep, which develops in four to six 90-min ultradian cycles, the decline of deep sleep and the increase of light sleep during the night are the most relevant contributions supplied by the conventional criteria to understand the structure of sleep(22-24). Our study showed that this holds true also in subjects with sleep disorders. The composition of the single sleep cycle varies in the course of the night - the period length of deep sleep decreases from the first to the last sleep cycle and at the same time light sleep and REM sleep undergo a progressive increase (Figure 1). But the question to us was how all this relates to the person’s sense of rest in the morning. The importance of deep sleep for the subjective sense of rest after the sleep was shown as a significant negative correlation between Pittsburgh sleep quality index (PSQI) and deep sleep (N4) amount (r = -0.3; p < 0.05) (Figure 2). This was in accordance with similar previous studies by other authors (5,25). And this is not a static effect. During the course of night - going from the first to the last sleep cycle - this relation gets weaker, indicating the importance of initial sleep cycles to the overall sleep quality sense (Figure 3). From all the three arousal types that we have studied MAI in TST showed the highest correlation with PSQI (r = 0.42; p = 0.001). VAI in TST showed negative correlation with PSQI and this means that the more vegetative arousals patient has, the better his sleep quality is. That was unexpected, but it could be that internally generated vegetative arousals to some extent play an important role in sleep regulation and express not negative sleep disturbances, but maintenance of internal body functions instead(9).
Zakevicius M, Liesiene V, Griksiene R, Masaitiene R, Ruksenas O^95 Table 3. Arousal indices in sleep stages. N1 N2 N3 N4 REM p F Significantly differing sleep stages Number of subjects 45 45 45 45 45 BAI 11.7 ± 9.3 19.0 ± 14.0 3.6 ± 4.0 0.7 ± 1.2 9.3 ± 9.4 < 0.05 2.275 (^) 2 > 4; 2 > REM; REM > 41 > 3; 1 > 4; 2 > 1; 2 > 3; MAI 11.1 ± 11.0 25.1 ± 21.3 4.1 ± 5.0 0.2 ± 0.5 12.9 ± 11.1 < 0.0001 3.702 1 > 4; 2 > 1; 2 > 3; 2 > 4; 2 > REM; REM > 3; REM > 4 VAI 6.1 ± 6.7 15.8 ± 15.6 2.5 ± 3.6 0.3 ± 0.6 7.3 ± 6.9 < 0.01 5.369 2 > 1; 2 > 3; 2 > 4; 2 > REM BAI: Behavioural arousal index; MAI: Microarousal index; VAI: Vegetative arousal index; N1, N2, N3, N4: Stages 1, 2, 3, 4 of non-rapid eye movement sleep; REM: Rapid eye movement sleep; p : Significance of inter cycle differences; F: F-ratio variance; Average ± SD. Figure 2. Pittsburgh sleep quality index correlations with conventional sleep parameters (N = 51). W: Wake; N1, N2, N3, N4: Stages 1, 2, 3, 4 of NREM (non-rapid eye movement sleep); REM: Rapid eye movement sleep. Figure 3. Pittsburgh sleep quality index correlations with light sleep and deep sleep duration in different sleep cycles (N = 44). LS: Light sleep; DS: Deep sleep; REM: Rapid eye movement. AIs dynamics during the night is closely related to the duration of sleep stages in each sleep cycle. MAI corre- lations with PSQI increase from cycle to cycle, but it is not significant and is mainly related to increasing proportion of light sleep in each sleep cycle and especially N2. Correla- tions between BAI, VAI and PSQI become more negative over the night in parallel with decreasing amount of deep sleep in each sleep cycle (Figure 5). This negative trend Figure 4. Pittsburgh sleep quality index correlations with different type arousals in sleep cycles (N = 46). BAI: Behavioural arousal index; MAI: Microarousal index; VAI: Vegetative arousal index. Figure 5. Pittsburgh sleep quality index correlations with different type arousals in sleep cycles (N = 46). LS %: Percentage of light sleep; DS %: Percentage of deep sleep; BAI: Behavioural arousal index; MAI: Microarousal index; VAI: Vegetative arousal index; L: Left hand side axis; R: Right hand side axis. is similar to the negative correlations between PSQI and VAI in TST. That could be related to the maintenance and preparation of internal body functions before the morning time awakening. Not significant AI differences between sleep cycles (Table 2) and significant AI differences between sleep stages (Table 3) sug- gested that developments of human sleep within the single sleep cycle are more important for the sleep quality than the changes between sleep cycles. Factorial ANOVA confirmed that the sleep stage and the arousal type were significant factors for the AI values, whereas the sleep cycle was not (see above in Subjective sleep quality ).
Zakevicius M, Liesiene V, Griksiene R, Masaitiene R, Ruksenas O^97