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Short sleeping time and psychobiological responses to acute stress
International Journal of Psychophysiology 78 (2010) 209–214
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International Journal of Psychophysiology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j p s yc h o
Short sleeping time and psychobiological responses to acute stress Hisayoshi Okamura a,⁎, Akira Tsuda a,b, Jumpei Yajima a,c, Hamer Mark d, Satoshi Horiuchi e, Natsuki Toyoshima e, Toyojirou Matsuishi a,f a
Cognitive and Molecular Institute of Brain Diseases, Kurume University, Japan Department of Psychology, Kurume University, Japan Department of Human Studies, Beppu University, Japan d Psychobiology Group, University College London, UK e Graduate School of Psychology, Kurume University, Japan f Department of Pediatrics and Child Health, Kurume University School of Medicine, Japan b c
a r t i c l e
i n f o
Article history: Received 11 September 2009 Received in revised form 29 July 2010 Accepted 31 July 2010 Available online 6 August 2010 Keywords: Sleeping hours Psychobiological stress responses Mental stress test MHPG s-IgA
a b s t r a c t The aim of this study was to examine the association between self-reported sleeping time and psychobiological stress responses [3-Methoxy-4-hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA), perceived stress responses]. Thirty seven healthy men and women were recruited, and participants were divided according to the habitual number of hours of sleep as follows: adequate sleepers (AS) (6–8 h sleep per night regularly) (N = 22) and short sleepers (SS) (less than 5 h sleep per night regularly) (N = 15). Salivary MHPG, s-IgA and perceived stress were measured at baseline, immediately after task and recovery period. An increase in free-MHPG during the task period was observed in AS although freeMHPG increased only after the task period in SS. The level of s-IgA in both groups significantly increased during the task period, and quickly returned to a basal level during the recovery period. The results show that less than 5 h of sleep was associated with different responsiveness to the Stroop color word conflict task compared to sufficient sleep, especially in the NA system. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Sleep has important homeostatic functions and sleep deprivation is a stressor that has consequences for the brain, as well as many body systems. Sleep problems are associated with the cognitive function, chronic illness and reduced mental health and premature mortality (Strine and Chapman, 2005; Foley et al., 2004; Roberts et al., 2000). Numerous studies have proposed that adequate sleep (AS) for adults is defined as 6–8 h per night on a regular basis (Lorton et al., 2006; Washio et al., 2004; Vgontzas et al., 2004). Sleeping less or more than 6–8 h day is associated with an increased risk of coronary heart disease, hypertension, and diabetes (Gottlieb et al., 2005; Ayas et al., 2003; Cappuccio et al., 2007). Previous studies demonstrated the number of hours of sleep to be an important indicator of health and well-being. We recently demonstrated that self-reported sleeping time relates to perceived health and change in psychoneuroimmunological responses under the daily circumstances (Okamura et al., 2009). Furthermore, Roth and Ancoli-Israel (1999) reported that long-term sleep deprivation results in an impaired concentration, an impaired memory and a decreased ability to accomplish daily tasks. In addition to these deficits, ⁎ Corresponding author. Cognitive and Molecular Institute of Brain Diseases, Kurume University, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan. Tel.: + 81 942 31 7581; fax: + 81 942 31 7911. E-mail address: [email protected] (H. Okamura). 0167-8760/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2010.07.010
long-term sleep deprivation has been reported to be associated with dysfunctional immune systems (Palma et al., 2007), particularly in depressive participants with sleep disturbance (Motivala et al., 2005). A recent experiment study by Capaldi et al. (2005) revealed blunted cortisol reactivity to an experimental stressor among participants with poor self-reported sleep quality in comparison to those with better sleep quality, although self-reported sleep quantity (hours of sleep) was not related to cortisol activity. Wright et al. (2007) also reported that individuals with objectively assessed poor sleep had a blunted response to the experimental stressor, although no associations were found between cortisol activity and self-reported sleep variables. However, compared to the number of epidemiological studies, few have examined relationship between self-reported sleeping time and psychobiological stress responses during mental stress testing. Allostasis and the allostatic load are relatively new concepts, which have been proposed to explain the physiological responses to chronic stress (McEwen, 2003). According to this model, allostasis is an extension of the concept of homeostasis, which represents the chronic adaptation process of complex physiological systems to physical, psychosocial and environmental challenges (Karlamangle et al., 2002; McEwen, 2002). Perceived stress initiates the person's physiological and behavioral responses and subsequently these responses lead to allostasis in various system including the sympathetic-adrenal medullary (SAM) system and hypothalamic-pituitary -adrenal (HPA) axis and cardiovascular, metabolic, neural, endocrine and immune
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systems. Repeated and cumulative allostasis over time causes an allostatic load (McEwen, 1998, 2006a) and frequent or chronic challenges produce dysregulation of several major physiological systems, including the HPA axis, SAM system and the immune system (Schulkin, 2004). In addition, whether sleep deprivation is due to anxiety, depression, or a hectic lifestyle, there are consequences of chronic sleep deprivation that impair the brain functions and contribute to allostatic load throughout the body (McEwen, 2006b). Habitual sleeping hours has been studied for its adverse effect on cognitive functioning and perceived stress over the day, but relatively little is known about its effect on mood, performance and biological responses [3-Methoxy-4-hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA)] under the acute stress condition. MHPG is a metabolite of noradrenaline. MHPG in plasma increases acutely in response to sympathetic activation such as exercise or acute mental stress and is unaffected by beta-blockade, suggesting that it is an indicator of central noradrenergic activity (Drici et al., 1991; Reuster et al, 2002; Hamer et al, 2007). Salivary free-MHPG has been shown to correlate both with concentrations in plasma (Yajima et al., 2001) and in cerebrospinal fluid (Reuster et al., 2002). In addition, the concentration of salivary free-MHPG is not effected by diurnal variation or salivary flow rate (Yajima et al., 2001). IgA is the primary antibody at mucosal surfaces (Bosch et al., 2002; Underdown and Mestecky, 1999) and individuals with reduced s-IgA in their saliva are more susceptible to upper respiratory tract infections (Evans et al., 1995). Salivary s-IgA becomes a focus of interest in psychoneuroimmunological research since it has been shown to be sensitive to variations in subjective and objective stress levels. Chronic psychosocial stresses are associated with reduction in s-IgA (Phillips et al., 2006; Gallagher et al., 2008), while humor (Harrison et al., 2000), relaxation (Green et al., 1988), and acute laboratory stressors, such as public speaking (Bristow et al., 1997) and mental arithmetic (Ring et al., 2002), appear to increase s-IgA. In this study, s-IgA was used as objective stress marker. The salivary measurement of free-MHPG and s-IgA is non-invasive and is neither inconvenient nor uncomfortable for participants. The aim of this study was to examine the association between sleeping time and psychobiological stress responses [3-Methoxy-4hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA), self-perceived mental workload]. In this study, the Stroop color word conflict task was selected as the mental stress test because this task is a very established stress task for assessing high-demand cognitive processing, including attention and executive control processes, via effects of stimulus conflict on psychomotor responses (Strike and Steptoe, 2003; Brydon et al., 2008). In addition, the Stroop color word conflict task requires both working memory and executive function, factors that are reported to be associated with the activation of noradrenergic neurones in the prefrontal cortex and immune function (Coull et al., 1997; Coull et al., 2001; Brydon et al., 2009). We hypothesized that chronic short self reported sleeping time would be associated with lower performance to task and greater psychobiological stress responses (increases MHPG, s-IgA, and self-perceived mental workload) to acute stress due to the allostatic load. These relationships were compared between AS and short sleepers (SS) using the experimental-field study paradigm. In this study, sleeping time was defined as time in bed (calculated from self -reported bedtime and rise time). Furthermore, we operationally defined 6 to 8 h of sleep as the AS group and less than 5 h of sleep as the SS group, according to Washio et al. (2004). 2. Methods Subjects: Thirty seven healthy men and women (mean age 18.6 ± 1.0 years) were recruited from a student population. Habitual sleeping time was evaluated using a Health and Behavior Survey (On average, how many hours of sleep do you get in a 24 h period
during past 4 weeks?) and participants were classified into two groups as follows at the field session: adequate sleepers (AS) (6–8 h sleep per night regularly) (N = 22) and short sleepers (SS) (less than 5 h sleep per night regularly) (N = 15). All participants gave full informed consent to participate in the study and ethical approval was obtained from the ethics Committee of Kurume University. Procedure: Before the experimental session, the participants completed the General Health Questionnaire (GHQ-28) (Goldberg and Hillier, 1979). The experimental session had three parts; a baseline period of 10 min, a 9 min task period and a post task period of 10 min. The participants were invited to relax during the baseline and post-task periods. Each period was followed by saliva sampling and mood assessments. Saliva samples were collected using Salivettes (SARSTEDT, Sarsted Numbrecht, Netherlands) for a period of 2 min (without moving the jaw or stimulating saliva production in any way). This study was performed in an air-conditioned room in the afternoon beginning at 1:30 pm. Participants were requested to refrain from vigorous exercise, smoking, and food, caffeine, and alcohol intake for 2 h prior to session. Mental stress testing: The Stroop color word conflict task was administered by computer. A color name was presented in the central part of the screen either in the named or different color. Four color names were also presented at the bottom of the screen and the participant was required to respond with the color in which the target was displayed. The pace of the presentation varied randomly across the trial. Behavioral performance was assessed in terms of number of reactions, response time and perceptual sensitivity measures. Questionnaire: GHQ-28 was administered as a measure of psychological distress. It has 28 items that assess four sub-scales; somatic symptoms, anxiety and insomnia, social dysfunction and depression. The GHQ-28 was scored using the standard method (Goldberg and Hillier, 1979). Perceived stress and activation were assessed using each session using an adaptation of the Japanese UWIST mood adjective checklist (Okamura et al., 2004). This is based on the UWIST score developed by Mathews et al. (1990) and consists of 12 items that measure the fundamental dimensions of energetic arousal (EA) (feeling lively/active versus tired/sluggish), and tense arousal (TA) (feeling anxious/nervous versus relaxed/calm). Questions were rated on a four-point scale and scores were summed, so that higher EA and TA values reflect greater energetic arousal and tension, respectively. The NASA-TLX (Hart and Staveland, 1988) is a measure of perceived workload related to any task. The questionnaire comprises visual analog scale (100 mm) for six workload facets; Mental demand (how much mental and perceptual activity was required?), Physical demand (how much physical activity was required?), Temporal demand (how much time pressure did you feel due to the rate or pace at which the task elements occurs?), Effort (how hard did you have to work?), Perceived performance (how successful do you think you were in accomplishing), and Frustration (how much irritate and stress did you feel during task?). Item based on the NASA-TLX workload measure were included in post-task assessment as a further motivational construct. Measurement of biological responses: Saliva samples were frozen at −80°C until assayed. The concentration of MHPG was measured using gas chromatography mass spectrometry (Hitachi, Japan), as described by Yajima et al. (2001). The limit of detection of this assay was 0.55 ng/ml, with intra- and inter-assay coefficients of variation (CVs) of 3.95% and 5.70%, respectively. In addition, the concentration of s-IgA was measured using an Enzyme Immune Assay (E.I.A kit; MBL CO. Ltd.). The limit of detection of this assay was 0.06 μg/ml, with intra- and inter-assay CVs of 2.95% and 7.41%, respectively. 3. Statistics The date was analyzed using SPSS Statistical Package for the Social Science Version 11.0 J. The χ2 test was used to analyze differences in
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the group and gender differences. Student's t-tests were used to detect the differences in age, the scores of GHQ-28 and task performance between two groups. The perceived and biological responses to task were analyzed using repeated measures analyses of variance (ANOVA), which independent variables were group (AS and SS) as between subjects factor and periods (Baseline, Task, and Posttask) as within-subject factor. Also, salivary flow rate was assessed using two way (AS and SS × Baseline, Task, Post-task) ANOVA because of salivary s-IgA concentration is influenced by salivary flow (Jemmott and McClelland, 1989). Post hoc tests were conducted using Tukey's least significant difference test. The data are presented as the means ± standard deviation (SD).
4.5. Salivary flow rate
4. Results
Fig. 3 shows the changes in MHPG and Fig. 4 shows the changes in s-IgA. There was a significant interaction in the MHPG between the group and period (F(2, 70) = 3.20, p b 0.05). The post hoc test revealed that MHPG levels in the AS significantly increased during the task (p b 0.05), on the other hand, those in the SS group increased during the post task (p b 0.05), but not during the task. In addition, the SS group showed a significantly higher level of MHPG during recovery than that of the AS group (p b 0.05). The secretion rate of s-IgA was calculated by multiplying the concentration of s-IgA and the amount of saliva for statistical analyses. This measure indicates the s-IgA concentration × volume of saliva/ min. The main significant effects were observed for period in the levels of s-IgA in the both AS and SS groups increased during the task (F(2, 66) = 8.28, p b 0.01). Post hoc comparisons indicated the level of s-IgA in each groups significantly increased during the task (p b 0.05). There was no group effect and no significant interactions were detected.
4.1. Group characteristics The group characteristics are summarized in Table 1. The average number of hours of sleep in SS was significantly shorter than that of AS (t = −9.17, df = 35, p b 0.01). In addition, the score of somatic symptoms on the GHQ-28 in SS was significantly higher than that of AS (t = 2.19, df = 35, p b 0.05). However, there were no group differences in the scores of anxiety–insomnia, social dysfunction and depression on the GHQ-28. The groups did not differ significantly in age or gender. 4.2. Mood and sleeping hours Fig. 1 shows the changes in TA and EA for AS and SS groups, respectively. The main significant effects were observed for period in the analysis of TA (F(2, 70) = 15.45, p b 0.01) and EA(F(2, 70) = 8.59, p b 0.01). Post hoc comparisons indicated the TA scores in each groups significantly increased during the task (p b 0.01), on the other hand, the EA scores in each groups significantly decreased during the task (p b 0.05). There was no group effect in relation to TA and EA scores. In addition, no significant interactions were detected for TA and EA. 4.3. NASA-TLX Fig. 2 shows the NASA-TLX scores. The levels of Mental demand and Temporal demand in SS tended to be higher than those of AS (t = 1.71, df = 35, p b 0.10; t = 1.69, df = 35, and p b 0.10, respectively). However, no significant differences were observed for the other scales. 4.4. Task performance There were no group differences in the number of reactions, response time or perceptual sensitivity measures.
Table 1 Characteristics of sujects. Characteristics
Adequate (n = 22)
Short sleepers (n = 15)
Age Women (%) Sleeping hours GHQ-28 Somatic symptoms Anxiety-insomnia Social dysfunction Depression
20.5 ± 4.8 15 (68.2) 7.2 ± 0.6
19.9 ± 1.1 10 (66.7) 4.0 ± 1.0 **
2.3 ± 2.2 2.7 ± 2.3 1.0 ± 1.5 2.0 ± 2.7
3.7 ± 1.7 * 2.4 ± 1.9 1.1 ± 1.1 1.3 ± 2.1
Average age and GHQ scores of adequate sleepers and short sleepers were expressed as mean ± SD. Average hours of sleep in 1 month before of this study was summarized as the means± S. *p b 0.05, compared with adequate sleepers. **p b 0.01, compared with adequate sleepers.
The main significant effects were observed for period in the analysis of salivary flow rate (F(2, 70) = 11.53, p b 0.01). Post hoc comparisons indicated the salivary flow rate in each group significantly decreased during the task (p b 0.01). Furthermore, a significant main effect was observed for the groups (F(1, 33) = 5.81, p b 0.05), the flow rate of saliva in the SS group during the baseline, task and posttask periods were significantly higher than those of AS (each periods p b 0.05, respectively). 4.6. Biological responses
5. Discussion Based on the subjects' personal experience of sleep deprivation and then subsequently “getting a good night's sleep”, there can be little doubt that sleep plays a role in maintaining better mood and cognitive acuity, as well as in promoting physiological balance and resilience (McEwen, 2006b). These impressions are supported by investigations of the effects of sleeping time on the cognitive and psychobiological stress responses. This present study was designed to assess the relationship between self-reported sleeping time, psychobiological stress responses and performance during mental stress testing. The main finding of this study showed an association between sleep and psychobiological response patterns, especially 5 hours of sleep was associated with different NA responsiveness to the Stroop color word conflict task compared to sufficient sleep. There are many reports showing sleep deprivation to be associated with workload and workrelated demand (Arora et al., 2008; Kivistö et al., 2008; Akerstedt et al., 2004). Ellenbogen (2005) also reported that symptoms resulting from sleep loss include an impaired cognitive and behavioral performance, partly from diminished attention and arousal. Ban and Lee (2001) have shown that sleep deprivation is associated with impaired concentration in class among university students. In this study, the levels of Mental demand and Temporal demand in the SS group tended to be higher than those of the AS group. Our findings and those of previous studies, demonstrated that sleep deprivation is related to an increase in perceived workload as assessed by mental demand and temporal demand. However, there were no group differences in the task performance. Increases in objective sleepiness and performance lapses are associated with a shorter sleep time (Pack et al., 2006). Particularly, a short sleep time and chronic sleep loss produces a decline in the cognitive and behavioral performance on simple and long period tasks with no feedback on the result (Gillberg and Akkerstedt, 1998; Koslowsky and Babkoff, 1992). Inconsistencies between our results and previous studies may be explained by the
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Fig. 1. Tension arousal (TA) and Energy arousal (EA) scores on JUMACL (mean ± SE) at baseline, task and post-task periods in the Stroop task. Black circles (●) with a solid line is the change of TA scores in adequate sleepers (AS) and white circles (○) with dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline.
difference in the task and/or procedure. The Stroop color word conflict task used by this study provides immediate feedback and the pace of the presentation varied randomly across the trial. In addition, the task period was short. Therefore, there were apparently no group differences in the number of reactions, response time and perceptual sensitivity measure. Further studies will therefore be needed with regard to complex task performance. Higher NA nervous system activity and impaired immune function have been reported in subjects who have few hours of sleep or chronic sleep loss, including sleep disorders (Irwin et al., 1999; Takase et al., 2004; Lorton et al., 2006). In this study, the concentrations of freeMHPG in the students who had adequate sleep increased during the task period, and quickly returned to a basal level during the recovery period. On the other hand, in the students who had short sleep, freeMHPG increased significantly after the task period, but not during the task period. Furthermore, the basal concentrations of MHPG in the students with short sleep tended to be higher than students with adequate sleep and it was significantly higher during the recovery period. In addition to these findings, the level of s-IgA in both groups significantly increased during the task period, and quickly returned to a basal level during the recovery period. The results of our previous study had shown that salivary free-MHPG and s-IgA in healthy control subjects were increased by the Stroop color word conflict task, and quickly returned to a basal level during the recovery period (Yajima et al., 2002; Tsuda et al., 2003). The AS group in this study showed
similar changes in our past studies, suggesting that this group retained appropriate reactions to acute stress. In contrast, freeMHPG in the SS group showed different changes from those previously observed in healthy control subjects. This might lead to a chronic state of stress due to the allostatic load. These disturbances might lead to vulnerability in illness such as depression, anxiety disorder and stress-related disease. The results of this study confirmed the findings of a previous study which reported the long term consequences of sleep deprivation to constitute a form of allostatic load (McEwen, 2006b). It will be necessary to further comprehensively examine the effects of a long sleep time on psychobiological responses such as cardiovascular responses, psychoneuroendocrinological responses and perceived stress responses to acute and chronic stress including changes in cognitive-behavioral functioning. Willemsen et al. (2000) demonstrated that increased IgA concentration was influenced by task novelty. In this study also, the increased s-IgA concentration in both groups might be effected by the task novelty. In addition, some previous studies had shown that salivary flow is often correlated with change in concentration of s-IgA (e.g., Stone et al., 1987). Jemmott and McClelland (1989) had shown that sIgA concentrations decrease with increased salivary flow. In the present study, the flow rate of saliva in each group significantly decreased during the task. Therefore, there were apparently no group differences in change of s-IgA level. However, the flow rate of saliva in
Fig. 2. NASA-TLX scores (mean ± SE) in the Stroop task. The Black bar is the scores in adequate sleepers (AS) and the white bar is that in short sleepers (SS). † p b 0.10 compared with adequate sleepers.
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Fig. 3. The saliva levels of MHPG (mean ± SE) at baseline, Stroop task and post-task periods. Black circle (●) with the solid line is change of MHPG in adequate sleepers (AS) and the white circle (○) with the dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline, #p b 0.05 compared with adequate sleepers.
Fig. 4. The saliva levels of s-IgA (mean ± SE) at baseline, task and post-task periods in the Stroop task. Black circle (●) with the solid line is the change of IgA in adequate sleepers (AS) and the white circle (○) with the dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline.
the short sleepers was significantly higher than that of adequate sleepers throughout the experiment. In conclusion, the results of the present study provide evidence that less than 5 h of sleep was associated with different responsiveness to the Stroop color word conflict task compared to sufficient sleep, especially in the NA system. We have previously demonstrated that depressive symptoms are also associated with disturbed MHPG responses to mental stress (Hamer et al., 2007) it is necessary to further understand the causal pathways linking disturbed sleep, mental health, and psychobiological function. Finally, there were some limitations in this study. First, sleep duration was measured by self-report, which might not accurately reflect objective sleep times. Therefore, it is difficult to generalize our finding of this short sleeping time to insufficient short sleep or patients with insomnia. In addition, this study is lacking of any objective and subjective assessment of sleep quality. Our study focused only on the number of sleeping hours. Nevertheless, epidemiological evidence suggested that a simple, self-reported measure of sleeping time predicts future risk of mortality (e.g., see Ferrie et al., 2007). Thus simple measures of sleeping time do appear to have utility in predicting health outcomes. In order to further examine the effects of sleep on psychobiological responses as well as changes in cognitive-behavioral functioning in the future, it will be necessary to use the Pittsburgh Sleep Quality Index and Actigraph to conduct an investigation that takes the quality of sleep into consideration. Second, since there were apparently no group differences in the number of reactions, response time and perceptual sensitivity measures, further studies will be needed that employ more complex task performance such as the TSST.
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International Journal of Psychophysiology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j p s yc h o
Short sleeping time and psychobiological responses to acute stress Hisayoshi Okamura a,⁎, Akira Tsuda a,b, Jumpei Yajima a,c, Hamer Mark d, Satoshi Horiuchi e, Natsuki Toyoshima e, Toyojirou Matsuishi a,f a
Cognitive and Molecular Institute of Brain Diseases, Kurume University, Japan Department of Psychology, Kurume University, Japan Department of Human Studies, Beppu University, Japan d Psychobiology Group, University College London, UK e Graduate School of Psychology, Kurume University, Japan f Department of Pediatrics and Child Health, Kurume University School of Medicine, Japan b c
a r t i c l e
i n f o
Article history: Received 11 September 2009 Received in revised form 29 July 2010 Accepted 31 July 2010 Available online 6 August 2010 Keywords: Sleeping hours Psychobiological stress responses Mental stress test MHPG s-IgA
a b s t r a c t The aim of this study was to examine the association between self-reported sleeping time and psychobiological stress responses [3-Methoxy-4-hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA), perceived stress responses]. Thirty seven healthy men and women were recruited, and participants were divided according to the habitual number of hours of sleep as follows: adequate sleepers (AS) (6–8 h sleep per night regularly) (N = 22) and short sleepers (SS) (less than 5 h sleep per night regularly) (N = 15). Salivary MHPG, s-IgA and perceived stress were measured at baseline, immediately after task and recovery period. An increase in free-MHPG during the task period was observed in AS although freeMHPG increased only after the task period in SS. The level of s-IgA in both groups significantly increased during the task period, and quickly returned to a basal level during the recovery period. The results show that less than 5 h of sleep was associated with different responsiveness to the Stroop color word conflict task compared to sufficient sleep, especially in the NA system. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Sleep has important homeostatic functions and sleep deprivation is a stressor that has consequences for the brain, as well as many body systems. Sleep problems are associated with the cognitive function, chronic illness and reduced mental health and premature mortality (Strine and Chapman, 2005; Foley et al., 2004; Roberts et al., 2000). Numerous studies have proposed that adequate sleep (AS) for adults is defined as 6–8 h per night on a regular basis (Lorton et al., 2006; Washio et al., 2004; Vgontzas et al., 2004). Sleeping less or more than 6–8 h day is associated with an increased risk of coronary heart disease, hypertension, and diabetes (Gottlieb et al., 2005; Ayas et al., 2003; Cappuccio et al., 2007). Previous studies demonstrated the number of hours of sleep to be an important indicator of health and well-being. We recently demonstrated that self-reported sleeping time relates to perceived health and change in psychoneuroimmunological responses under the daily circumstances (Okamura et al., 2009). Furthermore, Roth and Ancoli-Israel (1999) reported that long-term sleep deprivation results in an impaired concentration, an impaired memory and a decreased ability to accomplish daily tasks. In addition to these deficits, ⁎ Corresponding author. Cognitive and Molecular Institute of Brain Diseases, Kurume University, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan. Tel.: + 81 942 31 7581; fax: + 81 942 31 7911. E-mail address: [email protected] (H. Okamura). 0167-8760/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2010.07.010
long-term sleep deprivation has been reported to be associated with dysfunctional immune systems (Palma et al., 2007), particularly in depressive participants with sleep disturbance (Motivala et al., 2005). A recent experiment study by Capaldi et al. (2005) revealed blunted cortisol reactivity to an experimental stressor among participants with poor self-reported sleep quality in comparison to those with better sleep quality, although self-reported sleep quantity (hours of sleep) was not related to cortisol activity. Wright et al. (2007) also reported that individuals with objectively assessed poor sleep had a blunted response to the experimental stressor, although no associations were found between cortisol activity and self-reported sleep variables. However, compared to the number of epidemiological studies, few have examined relationship between self-reported sleeping time and psychobiological stress responses during mental stress testing. Allostasis and the allostatic load are relatively new concepts, which have been proposed to explain the physiological responses to chronic stress (McEwen, 2003). According to this model, allostasis is an extension of the concept of homeostasis, which represents the chronic adaptation process of complex physiological systems to physical, psychosocial and environmental challenges (Karlamangle et al., 2002; McEwen, 2002). Perceived stress initiates the person's physiological and behavioral responses and subsequently these responses lead to allostasis in various system including the sympathetic-adrenal medullary (SAM) system and hypothalamic-pituitary -adrenal (HPA) axis and cardiovascular, metabolic, neural, endocrine and immune
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systems. Repeated and cumulative allostasis over time causes an allostatic load (McEwen, 1998, 2006a) and frequent or chronic challenges produce dysregulation of several major physiological systems, including the HPA axis, SAM system and the immune system (Schulkin, 2004). In addition, whether sleep deprivation is due to anxiety, depression, or a hectic lifestyle, there are consequences of chronic sleep deprivation that impair the brain functions and contribute to allostatic load throughout the body (McEwen, 2006b). Habitual sleeping hours has been studied for its adverse effect on cognitive functioning and perceived stress over the day, but relatively little is known about its effect on mood, performance and biological responses [3-Methoxy-4-hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA)] under the acute stress condition. MHPG is a metabolite of noradrenaline. MHPG in plasma increases acutely in response to sympathetic activation such as exercise or acute mental stress and is unaffected by beta-blockade, suggesting that it is an indicator of central noradrenergic activity (Drici et al., 1991; Reuster et al, 2002; Hamer et al, 2007). Salivary free-MHPG has been shown to correlate both with concentrations in plasma (Yajima et al., 2001) and in cerebrospinal fluid (Reuster et al., 2002). In addition, the concentration of salivary free-MHPG is not effected by diurnal variation or salivary flow rate (Yajima et al., 2001). IgA is the primary antibody at mucosal surfaces (Bosch et al., 2002; Underdown and Mestecky, 1999) and individuals with reduced s-IgA in their saliva are more susceptible to upper respiratory tract infections (Evans et al., 1995). Salivary s-IgA becomes a focus of interest in psychoneuroimmunological research since it has been shown to be sensitive to variations in subjective and objective stress levels. Chronic psychosocial stresses are associated with reduction in s-IgA (Phillips et al., 2006; Gallagher et al., 2008), while humor (Harrison et al., 2000), relaxation (Green et al., 1988), and acute laboratory stressors, such as public speaking (Bristow et al., 1997) and mental arithmetic (Ring et al., 2002), appear to increase s-IgA. In this study, s-IgA was used as objective stress marker. The salivary measurement of free-MHPG and s-IgA is non-invasive and is neither inconvenient nor uncomfortable for participants. The aim of this study was to examine the association between sleeping time and psychobiological stress responses [3-Methoxy-4hydroxyphenylglycol (MHPG) and Secretory immunoglobulin A (IgA), self-perceived mental workload]. In this study, the Stroop color word conflict task was selected as the mental stress test because this task is a very established stress task for assessing high-demand cognitive processing, including attention and executive control processes, via effects of stimulus conflict on psychomotor responses (Strike and Steptoe, 2003; Brydon et al., 2008). In addition, the Stroop color word conflict task requires both working memory and executive function, factors that are reported to be associated with the activation of noradrenergic neurones in the prefrontal cortex and immune function (Coull et al., 1997; Coull et al., 2001; Brydon et al., 2009). We hypothesized that chronic short self reported sleeping time would be associated with lower performance to task and greater psychobiological stress responses (increases MHPG, s-IgA, and self-perceived mental workload) to acute stress due to the allostatic load. These relationships were compared between AS and short sleepers (SS) using the experimental-field study paradigm. In this study, sleeping time was defined as time in bed (calculated from self -reported bedtime and rise time). Furthermore, we operationally defined 6 to 8 h of sleep as the AS group and less than 5 h of sleep as the SS group, according to Washio et al. (2004). 2. Methods Subjects: Thirty seven healthy men and women (mean age 18.6 ± 1.0 years) were recruited from a student population. Habitual sleeping time was evaluated using a Health and Behavior Survey (On average, how many hours of sleep do you get in a 24 h period
during past 4 weeks?) and participants were classified into two groups as follows at the field session: adequate sleepers (AS) (6–8 h sleep per night regularly) (N = 22) and short sleepers (SS) (less than 5 h sleep per night regularly) (N = 15). All participants gave full informed consent to participate in the study and ethical approval was obtained from the ethics Committee of Kurume University. Procedure: Before the experimental session, the participants completed the General Health Questionnaire (GHQ-28) (Goldberg and Hillier, 1979). The experimental session had three parts; a baseline period of 10 min, a 9 min task period and a post task period of 10 min. The participants were invited to relax during the baseline and post-task periods. Each period was followed by saliva sampling and mood assessments. Saliva samples were collected using Salivettes (SARSTEDT, Sarsted Numbrecht, Netherlands) for a period of 2 min (without moving the jaw or stimulating saliva production in any way). This study was performed in an air-conditioned room in the afternoon beginning at 1:30 pm. Participants were requested to refrain from vigorous exercise, smoking, and food, caffeine, and alcohol intake for 2 h prior to session. Mental stress testing: The Stroop color word conflict task was administered by computer. A color name was presented in the central part of the screen either in the named or different color. Four color names were also presented at the bottom of the screen and the participant was required to respond with the color in which the target was displayed. The pace of the presentation varied randomly across the trial. Behavioral performance was assessed in terms of number of reactions, response time and perceptual sensitivity measures. Questionnaire: GHQ-28 was administered as a measure of psychological distress. It has 28 items that assess four sub-scales; somatic symptoms, anxiety and insomnia, social dysfunction and depression. The GHQ-28 was scored using the standard method (Goldberg and Hillier, 1979). Perceived stress and activation were assessed using each session using an adaptation of the Japanese UWIST mood adjective checklist (Okamura et al., 2004). This is based on the UWIST score developed by Mathews et al. (1990) and consists of 12 items that measure the fundamental dimensions of energetic arousal (EA) (feeling lively/active versus tired/sluggish), and tense arousal (TA) (feeling anxious/nervous versus relaxed/calm). Questions were rated on a four-point scale and scores were summed, so that higher EA and TA values reflect greater energetic arousal and tension, respectively. The NASA-TLX (Hart and Staveland, 1988) is a measure of perceived workload related to any task. The questionnaire comprises visual analog scale (100 mm) for six workload facets; Mental demand (how much mental and perceptual activity was required?), Physical demand (how much physical activity was required?), Temporal demand (how much time pressure did you feel due to the rate or pace at which the task elements occurs?), Effort (how hard did you have to work?), Perceived performance (how successful do you think you were in accomplishing), and Frustration (how much irritate and stress did you feel during task?). Item based on the NASA-TLX workload measure were included in post-task assessment as a further motivational construct. Measurement of biological responses: Saliva samples were frozen at −80°C until assayed. The concentration of MHPG was measured using gas chromatography mass spectrometry (Hitachi, Japan), as described by Yajima et al. (2001). The limit of detection of this assay was 0.55 ng/ml, with intra- and inter-assay coefficients of variation (CVs) of 3.95% and 5.70%, respectively. In addition, the concentration of s-IgA was measured using an Enzyme Immune Assay (E.I.A kit; MBL CO. Ltd.). The limit of detection of this assay was 0.06 μg/ml, with intra- and inter-assay CVs of 2.95% and 7.41%, respectively. 3. Statistics The date was analyzed using SPSS Statistical Package for the Social Science Version 11.0 J. The χ2 test was used to analyze differences in
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the group and gender differences. Student's t-tests were used to detect the differences in age, the scores of GHQ-28 and task performance between two groups. The perceived and biological responses to task were analyzed using repeated measures analyses of variance (ANOVA), which independent variables were group (AS and SS) as between subjects factor and periods (Baseline, Task, and Posttask) as within-subject factor. Also, salivary flow rate was assessed using two way (AS and SS × Baseline, Task, Post-task) ANOVA because of salivary s-IgA concentration is influenced by salivary flow (Jemmott and McClelland, 1989). Post hoc tests were conducted using Tukey's least significant difference test. The data are presented as the means ± standard deviation (SD).
4.5. Salivary flow rate
4. Results
Fig. 3 shows the changes in MHPG and Fig. 4 shows the changes in s-IgA. There was a significant interaction in the MHPG between the group and period (F(2, 70) = 3.20, p b 0.05). The post hoc test revealed that MHPG levels in the AS significantly increased during the task (p b 0.05), on the other hand, those in the SS group increased during the post task (p b 0.05), but not during the task. In addition, the SS group showed a significantly higher level of MHPG during recovery than that of the AS group (p b 0.05). The secretion rate of s-IgA was calculated by multiplying the concentration of s-IgA and the amount of saliva for statistical analyses. This measure indicates the s-IgA concentration × volume of saliva/ min. The main significant effects were observed for period in the levels of s-IgA in the both AS and SS groups increased during the task (F(2, 66) = 8.28, p b 0.01). Post hoc comparisons indicated the level of s-IgA in each groups significantly increased during the task (p b 0.05). There was no group effect and no significant interactions were detected.
4.1. Group characteristics The group characteristics are summarized in Table 1. The average number of hours of sleep in SS was significantly shorter than that of AS (t = −9.17, df = 35, p b 0.01). In addition, the score of somatic symptoms on the GHQ-28 in SS was significantly higher than that of AS (t = 2.19, df = 35, p b 0.05). However, there were no group differences in the scores of anxiety–insomnia, social dysfunction and depression on the GHQ-28. The groups did not differ significantly in age or gender. 4.2. Mood and sleeping hours Fig. 1 shows the changes in TA and EA for AS and SS groups, respectively. The main significant effects were observed for period in the analysis of TA (F(2, 70) = 15.45, p b 0.01) and EA(F(2, 70) = 8.59, p b 0.01). Post hoc comparisons indicated the TA scores in each groups significantly increased during the task (p b 0.01), on the other hand, the EA scores in each groups significantly decreased during the task (p b 0.05). There was no group effect in relation to TA and EA scores. In addition, no significant interactions were detected for TA and EA. 4.3. NASA-TLX Fig. 2 shows the NASA-TLX scores. The levels of Mental demand and Temporal demand in SS tended to be higher than those of AS (t = 1.71, df = 35, p b 0.10; t = 1.69, df = 35, and p b 0.10, respectively). However, no significant differences were observed for the other scales. 4.4. Task performance There were no group differences in the number of reactions, response time or perceptual sensitivity measures.
Table 1 Characteristics of sujects. Characteristics
Adequate (n = 22)
Short sleepers (n = 15)
Age Women (%) Sleeping hours GHQ-28 Somatic symptoms Anxiety-insomnia Social dysfunction Depression
20.5 ± 4.8 15 (68.2) 7.2 ± 0.6
19.9 ± 1.1 10 (66.7) 4.0 ± 1.0 **
2.3 ± 2.2 2.7 ± 2.3 1.0 ± 1.5 2.0 ± 2.7
3.7 ± 1.7 * 2.4 ± 1.9 1.1 ± 1.1 1.3 ± 2.1
Average age and GHQ scores of adequate sleepers and short sleepers were expressed as mean ± SD. Average hours of sleep in 1 month before of this study was summarized as the means± S. *p b 0.05, compared with adequate sleepers. **p b 0.01, compared with adequate sleepers.
The main significant effects were observed for period in the analysis of salivary flow rate (F(2, 70) = 11.53, p b 0.01). Post hoc comparisons indicated the salivary flow rate in each group significantly decreased during the task (p b 0.01). Furthermore, a significant main effect was observed for the groups (F(1, 33) = 5.81, p b 0.05), the flow rate of saliva in the SS group during the baseline, task and posttask periods were significantly higher than those of AS (each periods p b 0.05, respectively). 4.6. Biological responses
5. Discussion Based on the subjects' personal experience of sleep deprivation and then subsequently “getting a good night's sleep”, there can be little doubt that sleep plays a role in maintaining better mood and cognitive acuity, as well as in promoting physiological balance and resilience (McEwen, 2006b). These impressions are supported by investigations of the effects of sleeping time on the cognitive and psychobiological stress responses. This present study was designed to assess the relationship between self-reported sleeping time, psychobiological stress responses and performance during mental stress testing. The main finding of this study showed an association between sleep and psychobiological response patterns, especially 5 hours of sleep was associated with different NA responsiveness to the Stroop color word conflict task compared to sufficient sleep. There are many reports showing sleep deprivation to be associated with workload and workrelated demand (Arora et al., 2008; Kivistö et al., 2008; Akerstedt et al., 2004). Ellenbogen (2005) also reported that symptoms resulting from sleep loss include an impaired cognitive and behavioral performance, partly from diminished attention and arousal. Ban and Lee (2001) have shown that sleep deprivation is associated with impaired concentration in class among university students. In this study, the levels of Mental demand and Temporal demand in the SS group tended to be higher than those of the AS group. Our findings and those of previous studies, demonstrated that sleep deprivation is related to an increase in perceived workload as assessed by mental demand and temporal demand. However, there were no group differences in the task performance. Increases in objective sleepiness and performance lapses are associated with a shorter sleep time (Pack et al., 2006). Particularly, a short sleep time and chronic sleep loss produces a decline in the cognitive and behavioral performance on simple and long period tasks with no feedback on the result (Gillberg and Akkerstedt, 1998; Koslowsky and Babkoff, 1992). Inconsistencies between our results and previous studies may be explained by the
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Fig. 1. Tension arousal (TA) and Energy arousal (EA) scores on JUMACL (mean ± SE) at baseline, task and post-task periods in the Stroop task. Black circles (●) with a solid line is the change of TA scores in adequate sleepers (AS) and white circles (○) with dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline.
difference in the task and/or procedure. The Stroop color word conflict task used by this study provides immediate feedback and the pace of the presentation varied randomly across the trial. In addition, the task period was short. Therefore, there were apparently no group differences in the number of reactions, response time and perceptual sensitivity measure. Further studies will therefore be needed with regard to complex task performance. Higher NA nervous system activity and impaired immune function have been reported in subjects who have few hours of sleep or chronic sleep loss, including sleep disorders (Irwin et al., 1999; Takase et al., 2004; Lorton et al., 2006). In this study, the concentrations of freeMHPG in the students who had adequate sleep increased during the task period, and quickly returned to a basal level during the recovery period. On the other hand, in the students who had short sleep, freeMHPG increased significantly after the task period, but not during the task period. Furthermore, the basal concentrations of MHPG in the students with short sleep tended to be higher than students with adequate sleep and it was significantly higher during the recovery period. In addition to these findings, the level of s-IgA in both groups significantly increased during the task period, and quickly returned to a basal level during the recovery period. The results of our previous study had shown that salivary free-MHPG and s-IgA in healthy control subjects were increased by the Stroop color word conflict task, and quickly returned to a basal level during the recovery period (Yajima et al., 2002; Tsuda et al., 2003). The AS group in this study showed
similar changes in our past studies, suggesting that this group retained appropriate reactions to acute stress. In contrast, freeMHPG in the SS group showed different changes from those previously observed in healthy control subjects. This might lead to a chronic state of stress due to the allostatic load. These disturbances might lead to vulnerability in illness such as depression, anxiety disorder and stress-related disease. The results of this study confirmed the findings of a previous study which reported the long term consequences of sleep deprivation to constitute a form of allostatic load (McEwen, 2006b). It will be necessary to further comprehensively examine the effects of a long sleep time on psychobiological responses such as cardiovascular responses, psychoneuroendocrinological responses and perceived stress responses to acute and chronic stress including changes in cognitive-behavioral functioning. Willemsen et al. (2000) demonstrated that increased IgA concentration was influenced by task novelty. In this study also, the increased s-IgA concentration in both groups might be effected by the task novelty. In addition, some previous studies had shown that salivary flow is often correlated with change in concentration of s-IgA (e.g., Stone et al., 1987). Jemmott and McClelland (1989) had shown that sIgA concentrations decrease with increased salivary flow. In the present study, the flow rate of saliva in each group significantly decreased during the task. Therefore, there were apparently no group differences in change of s-IgA level. However, the flow rate of saliva in
Fig. 2. NASA-TLX scores (mean ± SE) in the Stroop task. The Black bar is the scores in adequate sleepers (AS) and the white bar is that in short sleepers (SS). † p b 0.10 compared with adequate sleepers.
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Fig. 3. The saliva levels of MHPG (mean ± SE) at baseline, Stroop task and post-task periods. Black circle (●) with the solid line is change of MHPG in adequate sleepers (AS) and the white circle (○) with the dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline, #p b 0.05 compared with adequate sleepers.
Fig. 4. The saliva levels of s-IgA (mean ± SE) at baseline, task and post-task periods in the Stroop task. Black circle (●) with the solid line is the change of IgA in adequate sleepers (AS) and the white circle (○) with the dashed line is that in short sleepers (SS). *p b 0.05 compared with baseline.
the short sleepers was significantly higher than that of adequate sleepers throughout the experiment. In conclusion, the results of the present study provide evidence that less than 5 h of sleep was associated with different responsiveness to the Stroop color word conflict task compared to sufficient sleep, especially in the NA system. We have previously demonstrated that depressive symptoms are also associated with disturbed MHPG responses to mental stress (Hamer et al., 2007) it is necessary to further understand the causal pathways linking disturbed sleep, mental health, and psychobiological function. Finally, there were some limitations in this study. First, sleep duration was measured by self-report, which might not accurately reflect objective sleep times. Therefore, it is difficult to generalize our finding of this short sleeping time to insufficient short sleep or patients with insomnia. In addition, this study is lacking of any objective and subjective assessment of sleep quality. Our study focused only on the number of sleeping hours. Nevertheless, epidemiological evidence suggested that a simple, self-reported measure of sleeping time predicts future risk of mortality (e.g., see Ferrie et al., 2007). Thus simple measures of sleeping time do appear to have utility in predicting health outcomes. In order to further examine the effects of sleep on psychobiological responses as well as changes in cognitive-behavioral functioning in the future, it will be necessary to use the Pittsburgh Sleep Quality Index and Actigraph to conduct an investigation that takes the quality of sleep into consideration. Second, since there were apparently no group differences in the number of reactions, response time and perceptual sensitivity measures, further studies will be needed that employ more complex task performance such as the TSST.
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