Abstract
Objective
To examine the relationship between sleep and resting Autonomic Nervous System (ANS) functioning in college students.
Participants
Participants were 141 undergraduate students (52 males) recruited from a large southeastern university during September-October 2017.
Methods
Participants completed self-report inventories (demographic and sleep characteristics). Resting state skin conductance (SC) and heart rate variability (HRV) were measured in a laboratory setting for ANS functioning.
Results
SC was positively associated with sleep quality (p=0.027), sleep latency (p=0.040), and use of sleep medication (p<0.001). Analyses yielded a negative association between the standard deviation of the normal-normal interval of heart beats (SDNN) and the self-reported amount of time to fall asleep each night (p=0.041). Sleep efficiency was negatively correlated with low frequency HRV (p=0.002).
Conclusions
Sleep components are associated with resting ANS activity, and targeted interventions focused on improved ANS functioning may benefit sleep quality in college students.
Keywords: Autonomic Balance, College Students, Sleep Behaviors, Well-being
The maintenance and promotion of health is vital to college student success. As such, one of the overarching goals of the Healthy Campus 2020 initiative outlined by the U.S. Department of Health and Human Services is to promote quality of life, healthy development, and positive health behaviors on college campuses. However, in a recent survey, the American College Health Association reported that students attributed stress (30%) and sleep difficulties (21%) as factors that negatively affected their academic performance (e.g., lower grade or dropped courses). For example, in an examination of 1,125 college students, sleep habits were explored in conjunction with academic performance and physical health factors. Results revealed that students who had poor sleep quality reported significantly more problems associated with physical and psychological health than those who reported better sleep quality. Moreover, academic and emotional stress have been cited as factors that contribute to poor sleep quality. 1,2 College students in particular are faced with innumerable stressors (e.g., academic performance, pressure to succeed, maintaining social relationships, dating, work-life balance, and post-graduation plans) and oftentimes sleep is sacrificed. 3,4
Sleep quality and duration are critical to cognitive, emotional, and physical well-being. 5–7 College students in particular are often subjected to irregular sleep schedules and often experience insufficient sleep and poor sleep quality. 8,9 Generally speaking, lack of sleep can hinder academic success 1 and lead to poor health outcomes such as obesity, 10 depression, 11 and other chronic diseases. 12 However, overall satisfaction with the sleep experience has been shown to be positively associated with well-being and positive affect. 13 For example, researchers have shown that sufficient and consistent sleep is linked to improved self-regulatory behaviors and decreased strain in college students. 14 Similarly, Lebensohn and colleagues reported that the two most significant wellness behaviors associated with higher well-being in medical students were exercise and restful sleep. 15 It is evident that sufficient sleep is important for overall well-being. However, research about the influence of sleep on resting autonomic nervous system (ANS) functioning in college students is lacking. In terms of the ANS, greater vagal activity (i.e. parasympathetic dominance) is viewed as conducive to health, whereas a dominant or overactive sympathetic branch proves to be detrimental to health. 16–18 The purpose of this study was to examine the extent to which college students are at risk for autonomic imbalances as a function of sleep.
Sleep deficits cause over-activity in the stress response systems, and this deficit may induce alterations in autonomic control. 19 For example, cardiovascular researchers have demonstrated that poor quality of sleep and sleep deprivation can produce a reduction in vagal tone, and thus disrupt the ANS ability to inhibit sympathetic dominance. 20–22 In a study of hypertensive patients, results revealed that poor sleep quality was associated with greater sympathetic nervous system (SNS) activation. 23 Because sleep deficiencies are associated with increased neuroendocrine activity, sleep deprivation in particular is considered a chronic stressor that often leads to negative consequences in the brain and body systems. 24,25
Modal responses of the ANS include cardiovascular, electrodermal, and respiratory changes. In the current study, we examined cardiovascular response via resting heart rate variability (HRV) and electrodermal response utilizing skin conductance (SC) functioning in healthy college students within our laboratory setting. SC provides a unique method for measuring autonomic functioning because alterations in sweating are mediated by cholinergic nerve activity. 26 SC responses are associated with increasing stress and anxiety. 27–29 In addition, elevated SC responses are associated with enhanced memory consolidation, emotional processing, and attention. 30 In a recent study, Liu and colleagues found college students who were sleep deprived displayed increased SC levels following a difficult perceptual task compared to their well-rested counterparts. 31 Thus, explorations into SC can provide important information about ANS arousal, specifically in relation to sleep. HRV is defined as the variance between consecutive heartbeats or the RR interval, 32 and the parasympathetic/vagal activity is associated with the high-frequency component of HRV. 33 Moreover, resting HRV is a biomarker for physical and psychological health. 34,35
Despite the well-documented link between sleep and overall well-being, understanding the effect of sleep on autonomic balance in college students is warranted. Therefore, the purpose of the current study was to examine the relationship between aspects of sleep and the aforementioned indices of ANS functioning at rest. Our central hypothesis was that aspects of sleep would show a positive association with autonomic function (operationalized by SC and HRV indices). Accordingly, less sympathetic activity (i.e. lower SC level, & minimal low frequency HRV power) would be reflective of better sleep quality.
Methods
Participants
Participants were 141 undergraduate students (52 males) currently enrolled in a large Southern predominately White university. In terms of ethnicity, 83.6% identified as White/European American, 7.9% identified as African-American, 6.4% identified as Asian-Americans, 0.7% identified as Latino(a)/Hispanic, 0.7% identified as Native American, and 0.7% identified as Middle Eastern. The age of participants ranged from 18 to 43 with a mean age of 20.72 (SD = 3.26). Participants were recruited using the Psychology department’s undergraduate research website. Inclusion criteria were as follows: (a) must be at least 18 years of age, and (b) no medical diagnosis of sleep disorders (e.g., narcolepsy, sleep apnea, or sleep terrors). This study was conducted during the 2017 Fall semester, and was approved by the University’s Institutional Review Board (IRB) prior to data collection.
Apparatus Used
A desktop Dell computer with a 22-inch color monitor was used to administer the survey and demographic sheet for each student as they individually came to the research lab. In an adjacent examination room, an additional Dell desktop computer with two 22-inch color monitors was used to run the physiological software program used in this study. The physiological measures (SC, HR, & HRV) were sampled via the multichannel Procomp InfinitiTM and Biograph software system (Thought Technology Ltd., Montreal, Canada). All sensor leads were connected to this 8-channel encoder, and each participant’s physiological data were exported into a data file. SC was measured using cuffs with sensors fastened around the middle and index fingers of the non-dominant hand. SC is measured in micro-Siemens units, and these data were collected at 32 Hz. A higher level of skin conductance response indicates a higher level of arousal.
HR (beats per minute) and HRV were measured via 3-lead electrode sensors placed on both forearms and the left wrist of the participant as outlined by the Thought Technology Manual, and these data were collected at 256 Hz. The raw inter-beat interval (IBI) data were analyzed in the time and frequency domains. More specifically, HRV was assessed via the following frequency domains: very low frequency (VLF) power between the limits of 0.003 Hz and 0.04 Hz, low frequency (LF) power in the range of 0.04 Hz and 0.15 Hz, high frequency (HF) power in the range of 0.15 Hz and 0.40 Hz, and LF/HF ratio. The HF component reflects parasympathetic cardiac control and LF reflects sympathetic/parasympathetic balance. 36 The time-domain measure included the standard deviation of normal-to-normal intervals (SDNN) of heart beats. In a recent study, borderline abnormal and abnormal SDNN readings were associated with increased risk of cardiovascular disease in middle aged adults.37
Measures
Demographic Questionnaire
A self-report questionnaire was used to obtain information about the demographics of our sample population. Information such as: age, race, sex, and classification in school were collected.
Sleep Questionnaire
Quality of sleep was measured using the Pittsburgh Sleep Quality Index (PSQI). 38 This self-administered questionnaire assesses quality of sleep during the previous month and contains 19 self-rated questions yielding seven components: subjective sleep quality (i.e., rating of sleep quality from poor to good), sleep latency (i.e., time it takes to fall asleep), sleep duration (i.e. how long asleep), sleep efficiency (i.e., percentage of time sleeping in a bed), sleep disturbance (i.e. how sleep is affected by disturbances), use of sleep medications (i.e. amount of usage), and daytime dysfunction (i.e. how sleep affects activities of daily living). Each component is scored from 0 to 3, yielding a global PSQI score between 0 and 21, with higher scores indicating lower quality of sleep. The PSQI is useful in identifying self-reported good sleepers and poor sleepers. A global PSQI score > 5 indicates that a person is a poor sleeper having severe difficulties in at least two areas or moderate difficulties in more than three areas.
Procedure
Upon arrival to the lab, all participants were asked to read and electronically sign the informed consent document. Once consent was given, participants were asked to complete a survey package (demographics and sleep quality). Once completed, participants were asked to sit quietly for 5 minutes prior to obtainment of physiological measures. After this acclimation period, participants were prepared for physiological recordings using the Thought Technology sensors interfaced with their software program. A measure of SC, HR, and HRV were measured simultaneously for 5 minutes in order to assess ANS functioning at rest. Physiological data were only collected at this time and no other measures were obtained. Participants were thanked for their cooperation and participation in this study.
Data analytic techniques
Data analyses for both the physiological and self-report data were performed using SPSS Version 25 for Windows. Artifacts (i.e. muscle tension, eye-blinks, etc.) from the physiological data were removed via the auto-edit functions of the Biograph (Physiological Suite) software program (Thought Technology Ltd., Montreal Canada). The frequency domains of the HRV indices were analyzed using fast Fourier transformation. The time domain of the HRV indices were computed from the IBI of the raw EKG signals. All alpha levels were set at 0.05. Demographic information is provided in Table 1. Bivariate Pearson correlations were computed in order to examine the association between aspects of sleep and resting ANS activity.
Table 1.
Descriptive Characteristics of Study Participants
| Study Variables | |
|---|---|
| Age (in years, M ± SD) | 20.716 ± 3.256 |
| Male (M; %) | 52; 36.9% |
| Female (M; %) | 89; 63.1% |
| White (M; %) | 117; 83.0% |
| Non-White (M; %) | 23; 16.3% |
| Av Sleep (in hours, M ± SD) | 6.720 ± 0.993 |
| Freshman (M; %) | 51; 36.2% |
| Sophomore (M; %) | 22; 15.6% |
| Junior (M; %) | 43; 30.5% |
| Senior (M; %) | 24; 17.0% |
Results
Demographics Variables
Due to the disproportion in racial identity in the current sample (i.e. 83% Caucasian), we excluded racial differences from analysis in this study. There were no significant differences by sex or classification status on the dependent measures. For the current study, we collapsed across race, sex, and classification status and explored this college student population linearly as a whole.
Components of Sleep
Table 2 contains the means and standard deviations for our sleep measure. The average PSQI global score for our college sample was 7.10 (SD = 2.64), and a score greater than 5 was indicative of poor sleep quality. The sleep components yielding the highest scores were sleep latency (M = 1.33, SD = 0.66) and sleep duration (M=1.28, SD = 0.97). Collectively, these results revealed that college students in our sample reported difficulty falling asleep and staying asleep; therefore, indicating insufficient daily sleep. Additionally, results revealed no significant differences in terms of sex for the components of sleep (see Table 3).
Table 2.
Means and Standard Deviations for Components of PSQI
| Mean | Std. Dev. | |
|---|---|---|
| Subjective Sleep Quality | 1.225 | 0.600 |
| Sleep Latency | 1.333 | 0.662 |
| Sleep Duration | 1.284 | 0.973 |
| Sleep Efficiency | 0.567 | 0.839 |
| Sleep Disturbance | 1.183 | 0.455 |
| Use of Sleep Medication | 0.437 | 0.863 |
| Daytime Dysfunction | 1.078 | 0.773 |
Note. Scores range from 0–3 with higher scores representing worse sleep quality.
Table 3.
Independent Samples T-Test of Components of PSQI by Sex
| Male | Female | ||||
|---|---|---|---|---|---|
| Mean | SD | Mean | SD | p | |
| Subjective Sleep Quality | 1.289 | 0.605 | 1.191 | 0.601 | 0.356 |
| Sleep Latency | 1.269 | 0.564 | 1.371 | 0.713 | 0.381 |
| Sleep Duration | 1.327 | 1.004 | 1.258 | 0.960 | 0.688 |
| Sleep Efficiency | 0.539 | 0.917 | 0.584 | 0.795 | 0.756 |
| Sleep Disturbance | 1.192 | 0.487 | 1.180 | 0.441 | 0.876 |
| Use of Sleep Medication | 0.442 | 0.826 | 0.438 | 0.891 | 0.978 |
| Daytime Dysfunction | 1.058 | 0.850 | 1.079 | 0.727 | 0.877 |
| Global PSQI | 7.115 | 2.784 | 7.101 | 2.567 | 0.975 |
Note. PSQI = Pittsburgh Sleep Quality Index
Skin Conductance
Changes in SC are presented in Fig. 1. After the acclimation period, SC was assessed at rest for 5 minutes. The SC mean was 2.978 μS (SD = 2.612), and most participants displayed a slight decrease in SC during baseline. Correlational analyzes yielded significant associations between SC at rest and components of sleep. More specifically, poor sleep quality was positively associated with increased SC levels (r = 0.187, p = 0.027). Likewise, higher sleep latency scores were positively associated with increased SC levels (r = 0.173, p = 0.040). Reliance upon sleep medication was also positively associated with increased SC levels (r = 0.306, p < 0.001). As expected, Global PSQI scores were positively associated with increased SC levels (r = 0.188, p = 0.026) (see Table 4).
Fig 1.
Histogram of Skin Conductance level (SCL) at rest for all study participants. The mean SCL is 2.98 μS for the current college student sample. SCL reflects the tonic level of electrical conductivity of the skin.
Table 4.
Correlation between Skin Conductance and Components of PSQI
| r | p | |
|---|---|---|
| Subjective Sleep Quality | 0.187* | 0.027 |
| Sleep Latency | 0.173* | 0.040 |
| Sleep Duration | 0.009 | 0.913 |
| Sleep Efficiency | −0.024 | 0.781 |
| Sleep Disturbance | −0.053 | 0.530 |
| Use of Sleep Medication | 0.306** | 0.000 |
| Daytime Dysfunction | 0.051 | 0.549 |
| Global PSQI | 0.188* | 0.026 |
Note.
Correlation is significant at the 0.05 level (2-tailed).
Correlation is significant at the 0.01 level (2-tailed).
Heart Rate Variability
Heart rate and HRV were examined in the current study. Baseline measures were assessed at the same time SC was assessed. The means and standard deviations for the cardiovascular variables are presented in Table 5. To examine the relationship between components of HRV (i.e., time and frequency domains) and aspects of sleep, correlational analyses were performed. Explorations into the relationship between HRV and sleep components showed that the amount of time reported to fall asleep each night (sleep latency) was negatively associated with SDNN (r = −0.173, p = 0.041) (see Fig. 2) suggesting that the longer it takes one to go to sleep, the lower one’s HRV. In addition, sleep efficiency was negatively correlated with LF% (r = −0.262, p = 0.002). Based on our findings, we suggest that better sleep efficiency is associated with reduced sympathetic activation. No other relationships demonstrated significance in terms of HRV and sleep components (p > 0.05).
Table 5.
Means and Standard Deviations for components of HRV
| Mean | Std. Dev. | |
|---|---|---|
| Heart Rate | 79.904 | 11.339 |
| VLF | 22.328 | 9.836 |
| LF | 42.453 | 10.486 |
| HF | 34.777 | 12.992 |
| LF/HF Ratio | 4.604 | 36.292 |
| SDNN | 45.942 | 29.030 |
Note. VLF = Very Low Frequency spectrum (0.003–0.04Hz), LF = Low Frequency spectrum (0.04–0.15Hz), HF = High Frequency spectrum (0.15–0.40Hz), LF/HF ratio = the ratio between of Low Frequency to High Frequency Heart Rate Variability, SNDD = standard deviation of normal-normal intervals.
Fig 2.
The Relationship between time to fall asleep (in mins) and standard deviation of the normal-normal (SDNN) interval component of Heart Rate Variability. Lower SDNN is reflective of worse health. This figure clearly shows that lower SDNN (i.e. worse heart health) is associated with longer times to fall asleep. Thus, longer times to fall asleep is not conducive to health.
Comment
Sufficient sleep is vital to overall well-being, but for many college students, a good night’s sleep is elusive. For this reason, this study was designed to provide insight into the relationship between components of sleep and ANS function at rest in healthy college students. Investigations into both sympathetic and parasympathetic branches of the ANS have shown that autonomic imbalances are precursors to disease formation and other health-related risks. 33,39,40 Findings from the current study indicate that both quality and quantity of sleep were associated with autonomic functioning at rest. Our principal findings revealed that: (a) college students routinely experienced difficulty in falling asleep and staying asleep which often led to the use of sleep medication, and (b) poor sleep quality and duration were associated with greater SC levels and lower HRV at rest. Collectively, our findings reveal that college students who are poor sleepers tend to display autonomic imbalances at rest. Moreover, they may be at increased risk for serious health problems later in life.
SC measures are routinely used to examine emotional reactivity 28,30,41,42 and general arousal. 26 In the current study, we found poor sleep quality, increased sleep medication use, and longer sleep latency times were associated with greater SC levels at rest. Our findings are similar to that of Liu and colleagues who reported sleep deprived college students to display higher SC reactivity to a stressful task compared to their well-rested counterparts. 31 Electrodermal activity such as SC is used to assess activity of the SNS in particular. 27 SNS dominance leads to autonomic imbalance, and places one at risk for chronic health disorders. 33,43,44 Therefore, the findings of the current study suggest self-reported that poor sleep quality and duration are associated with greater SNS dominance. Moreover, we argue that this autonomic imbalance interferes with sleep efficiency and the perceptions of a good night sleep. It is plausible that the strenuous life of a college student is reflective in a heightened stress response and the frequent use of sleep medication is an attempt to restore autonomic balance, and therefore sleep.
Another way to assess autonomic functioning is to examine HRV at rest. This approach has been widely used as a non-invasive tool to evaluate cardiovascular autonomic control in clinical and non-clinical populations 19 and can be defined as the physiological variation between successive beats of the heart, 45 with greater variability being associated with better health. 46 Researchers have shown that greater HRV is associated with more parasympathetic dominance in the ANS. 35 Sleep is also parasympathetically driven as transitions from wakefulness to sleep have shown to shift autonomic balance to that of a more parasympathetic tone. 47 Results of the current study indicated that increased sleep latency and decreased sleep efficiency were associated with lower HRV as measured by LF% and SDNN components. Both components of HRV reflect the relative dominance of each branch of the ANS. Researchers have shown that greater LF% is reflective of baroreceptors and primarily sympathetically driven, 48,49 while SDNN is a time domain and reflects the overall influence of both divisions of the ANS. 50 Our findings are consistent with findings of previous researchers who found reduced HRV associated with poor sleep quality. 51 Therefore, based upon our findings, we suggest that the longer it takes one to fall asleep, paired with less time in sleep, is associated with autonomic imbalance. Moreover, our findings lend support to previous researchers who suggested that sleep complications parlay into negative health outcomes. 23,25,53
Sleep has protective properties that bolster health; 23,25,52,53 however, insufficient sleep is a consequence to which many college students are subjected daily. 54 Sleep difficulties can manifest in college students due to a variety of reasons such as: deficits in time and stress management, 55 poor coping skills, 56 and fear of being in academic peril. 57 Based upon the results of the current study, we suggest that interventions focused on self-reported sleep difficulties in college students can be used as a non-invasive way to explore autonomic function and reduce the risk for health issues later in life.
Limitations
A few study limitations should be noted. First, we assessed sleep via self-report. Although the PSQI is a well-validated and often used measure of sleep quality, in both clinical and non-clinical populations 58,59 it is still subjective in nature. Objective measures such as actigraphy in conjunction with self-report measures of sleep are warranted. In this study, we correlated subjective measures of sleep with objective measures of health (SC and HRV). We found that individuals who reported difficulty in sleeping to also displayed higher resting SC levels and lower HRV. Moreover, this study was correlational in nature and causal inferences cannot be determined. It is plausible that disturbances in autonomic functioning cause sleep problems. Further studies are warranted to ferret out these findings. Finally, the current study did not have a very diverse sample in terms of race or classification status, thus a more diverse sample is warranted in order to determine if the current study’s findings hold true.
Conclusions
The current study was designed to investigate the relationship between components of self-reported sleep and indices of the ANS in relation to college students. We found several components of sleep (subjective sleep quality, sleep latency, and the use of sleep medication) were associated with autonomic functioning. More specifically, poorer sleep quality was associated with greater sympathetic dominance in college students. Sleep difficulties may either be the cause of, or the result of, increased sympathetic activation. This increased arousal may have caused students to take longer to fall sleep each night, which in turn, led students to consume more sleep medication. The maintenance and promotion of health and wellness is critical for college student success. Sufficient sleep is a vehicle for improved memory, cognitive performance, and overall health. 52,53,60 Although sleep medication may promote the process of going to sleep, students need to be educated about the pitfalls of reliance upon sleep medication. College administrators should focus on the implementation of brief psychoeducational courses 61 or other sleep hygiene intervention programs promoting sleep health and the benefits of sleep as a way of improving student well-being. 62–64
Acknowledgements
The authors would like to thank our undergraduate research assistant Shawnna Matthews for her assistance in data collection.
Funding: This work was supported by the National Institutes of Health Research Grants [MH59839 and MH115470].
Footnotes
Conflicts of interest disclosure
The authors have no conflicts of interest to report. The authors confirm that the research presented in this manuscript meet the ethical guidelines outlined by the University’s Institutional Review Board and the National Institutes of Health.
References
- 1.Gaultney JF. The prevalence of sleep disorders in college students: impact on academic performance. J Am Coll Health. 2010;59(2):91–97. doi: 10.1080/07448481.2010.483708. PMID:20864434. [DOI] [PubMed] [Google Scholar]
- 2.Lund HG, Reider BD, Whiting AB, Prichard JR. Sleep patterns and predictors of disturbed sleep in a large population of college students. J Adolesc. Health. 2010;46(2):124–32. doi: 10.1016/j.jadohealth.2009.06.016. [DOI] [PubMed] [Google Scholar]
- 3.Chen MY, Wang EK, Jeng YJ. Adequate sleep among adolescents is positively associated with health status and health-related behaviors. BMC Public Health. 2006;6(1):59. doi: 10.1186/1471-2458-6-59. PMID:16524482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Peach H, Gaultney JF, Reeve CL. Sleep characteristics, body mass index, and risk for hypertension in young adolescents. J Youth Adolesc. 2015;44(2):271–284. doi: 10.1007/s10964-014-0149-0. [DOI] [PubMed] [Google Scholar]
- 5.Datta S Phasic Pontine-Wave (P-Wave) Generation: Cellular-Molecular-Network Mechanism and Functional Significance In Sleep and Brain Activity. 2012;Chapter 7. (pp. 147–164). doi: 10.1016/B978-0-12-384995-3.00007-1. [DOI] [Google Scholar]
- 6.Datta S, Oliver MD. Cellular and Molecular Mechanisms of REM Sleep Homeostatic Drive: A Plausible Component for Behavioral Plasticity. Front. Neural Circuits 2017;11:63. doi: 10.3389/fncir.2017.00063. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Kamdar BB, Needham DM, Collop NA. Sleep deprivation in critical illness: its role in physical and psychological recovery. J Intens Care Med. 2012;27(2):97–111. doi: 10.1177/0885066610394322. PMID:21220271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Galambos NL, Vargas Lascano DI, Howard AL, Maggs JL. Who sleeps best? Longitudinal patterns and covariates of change in sleep quantity, quality, and timing across four university years. Behav. Sleep Med. 2013;11(1):8–22. doi: 10.1080/15402002.2011.596234. [DOI] [PubMed] [Google Scholar]
- 9.Lund HG, Reider BD, Whiting AB, Prichard JR. Sleep patterns and predictors of disturbed sleep in a large population of college students. J Adolesc Health. 2010;46(2):124–132. doi: 10.1016/j.jadohealth.2009.06.016. [DOI] [PubMed] [Google Scholar]
- 10.Fatima Y, Doi SA, Mamun AA. Sleep quality and obesity in young subjects: a meta-analysis. Obesity Reviews. 2016;17(11):1154–1166. doi: 10.1111/obr.12444. [DOI] [PubMed] [Google Scholar]
- 11.Alvaro PK, Roberts RM, Harris JK. A systematic review assessing bidirectionality between sleep disturbances, anxiety, and depression. Sleep. 2013:36(7):1059–1068. doi: 10.5665/sleep.2810. PMID: 23814343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Weitzenblum E, Chaouat A. Sleep and chronic obstructive pulmonary disease. Sleep Med Reviews. 2004;8(4):281–294. doi: 10.1016/j.smrv.2004.03.006. [DOI] [PubMed] [Google Scholar]
- 13.Steptoe A, O’Donnell K, Marmot M, Wardle J. Positive affect, psychological well-being, and good sleep. J Psychosomatic Res. 2008;64(4):409–415. doi: 10.1016/j.jpsychores.2007.11.008. [DOI] [PubMed] [Google Scholar]
- 14.Barber LK, Munz DC. Consistent‐sufficient sleep predicts improvements in self‐regulatory performance and psychological strain. Stress & Health. 2011;27(4):314–324. doi: 10.1002/smi.1364. [DOI] [Google Scholar]
- 15.Lebensohn P, Dodds S, Benn R, Brooks AJ, Birch M. Resident wellness behaviors. Fam Med. 2013;45(8):541–549. PMID:24129866. [PubMed] [Google Scholar]
- 16.Parati G, Esler M. The human sympathetic nervous system: its relevance in hypertension and heart failure. Euro Heart J. 2012;33(9):1058–1066. doi: 10.1093/eurheartj/ehs041. [DOI] [PubMed] [Google Scholar]
- 17.Shaffer F, McCraty R, Zerr CL. A healthy heart is not a metronome: an integrative review of the heart’s anatomy and heart rate variability. Front Psychol. 2014;5:1040. doi: 10.3389/fpsyg.2014.01040. PMID:25324790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Wulsin L, Herman J, Thayer JF. Stress, Autonomic Imbalance, and the Prediction of Metabolic Risk: A Model and a Proposal for Research. Neurosci & Biobehav Reviews. 2017; 86:12–20. doi: 10.1016/j.neubiorev.2017.12.010. [DOI] [PubMed] [Google Scholar]
- 19.Tobaldini E, Costantino G, Solbiati M, Cogliati C, Kara T, Nobili L, Montano N. Sleep, sleep deprivation, autonomic nervous system and cardiovascular diseases. Neurosci & Biobehav Reviews. 2017;74:321–329. doi: 10.1016/j.neubiorev.2016.07.004. [DOI] [PubMed] [Google Scholar]
- 20.Goldstein-Piekarski AN, Greer SM, Saletin JM, Walker MP. Sleep deprivation impairs the human central and peripheral nervous system discrimination of social threat. J Neurosci. 2015;35(28): 10135–10145. doi: 10.1523/JNEUROSCI.5254-14.2015. PMID:26180190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Sato M, Yasuhara Y, Tanioka T, Iwasa Y, Miyake M, Yasui T, Tomotake M, Kobayashi H, Locsin RC. Measuring quality of sleep and autonomic nervous function in healthy Japanese women. Neuropsychi Disease and Treatment. 2014;10:89–96. doi: 10.2147/NDT.S56827. PMID: 24465128. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Zhong X, Hilton HJ, Gates GJ, Jelic S, Stern Y, Bartels MN, DeMeersman RE, Basner RC. Increased sympathetic and decreased parasympathetic cardiovascular modulation in normal humans with acute sleep deprivation. J Applied Phys. 2005;98(6):2024–2032. doi: 10.1152/japplphysiol.00620.2004. [DOI] [PubMed] [Google Scholar]
- 23.Huang Y, Mai W, Hu Y, Wu Y, Song Y, Qiu R, Dong Y, Kuang J. Poor sleep quality, stress status, and sympathetic nervous system activation in nondipping hypertension. Blood Pressure Monitoring. 2011;16(3):117–123. doi: 10.1097/MBP.0b013e328346a8b4. [DOI] [PubMed] [Google Scholar]
- 24.McEwen BS. Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load. Metabolism-Clinical and Exper. 2006;55:S20–S23. doi: 10.1016/j.metabol.2006.07.008. [DOI] [PubMed] [Google Scholar]
- 25.McEwen BS, Karatsoreos IN. Sleep deprivation and circadian disruption: stress, allostasis, and allostatic load. Sleep Med Clinics. 2015;10(1):1–10. doi: 10.1016/j.jsmc.2014.11.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Jacobs SC, Friedman R, Parker JD, Tofler GH, Jimenez AH, Muller JE, Benson H, Stone PH. Use of skin conductance changes during mental stress testing as an index of autonomic arousal in cardiovascular research. Am Heart J. 1994;128(6):1170–1177. doi: 10.1016/0002-8703(94)90748-X. [DOI] [PubMed] [Google Scholar]
- 27.Andrews J, Ali N, Pruessner JC. Reflections on the interaction of psychogenic stress systems in humans: the stress coherence/compensation model. Psychoneuroendocrinology. 2013;38(7):947–961. doi: 10.1016/j.psyneuen.2013.02.010. [DOI] [PubMed] [Google Scholar]
- 28.Oliver MD, Datta S, Baldwin DR. A sympathetic nervous system evaluation of obesity stigma. PloS One. 2017;12(10):e0185703. doi: 10.1371/journal.pone.0185703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Storm H Skin conductance and the stress response from heel stick in preterm infants. Archives Disease Childhood-Fetal Neonat. Ed 2000;83(2):F143–F147. doi: 10.1136/fn.83.2.F143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.LaBar KS, Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews Neurosci. 2006;7(1):54–64. doi: 10.1038/nrn1825. [DOI] [PubMed] [Google Scholar]
- 31.Liu JC, Verhulst S, Massar SA, Chee MW. Sleep deprived and sweating it out: the effects of total sleep deprivation on skin conductance reactivity to psychosocial stress. Sleep. 2015;38(1):155–159. doi: 10.5665/sleep.4346. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Berntson GG, Thomas Bigger J, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, DER MOLEN MW. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34(6):623–648. doi: 10.1111/j.1469-8986.1997.tb02140.x. [DOI] [PubMed] [Google Scholar]
- 33.Thayer JF, Yamamoto SS, Brosschot JF. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int. J Cardiology. 2010;141(2):122–131. doi: 10.1016/j.ijcard.2009.09.543. [DOI] [PubMed] [Google Scholar]
- 34.Acharya UR, Joseph KP, Kannathal N, Lim CM, Suri JS. Heart rate variability: A review. Med Bio Eng Comput. 2006;44(12):1031–1051. doi: 10.1007/s11517-006-0119-0. [DOI] [PubMed] [Google Scholar]
- 35.Thayer JF, Åhs F, Fredrikson M, Sollers III JJ, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci & Biobehav Reviews. 2012;36(2):747–756. doi: 10.1016/j.neubiorev.2011.11.009. [DOI] [PubMed] [Google Scholar]
- 36.Stein PK, Kleiger RE. Insights from the study of heart rate variability. Annual Review Med 1999;50:249–261. doi: 10.1146/annurev.med.50.1.249. PMID: 10073276. [DOI] [PubMed] [Google Scholar]
- 37.O’neal WT, Salahuddin T, Broughton ST, Soliman EZ. Atrial fibrillation and cardiovascular outcomes in the elderly. Pacing Clinical Electrophys. 2016;39(9):907–913. doi: 10.1111/pace.12907. [DOI] [PubMed] [Google Scholar]
- 38.Carpenter JS, Andrykowski MA. Psychometric evaluation of the Pittsburgh sleep quality index. J Psychosomatic Res. 1998;45(1):5–13. doi: 10.1016/S0022-3999(97)00298-5. [DOI] [PubMed] [Google Scholar]
- 39.Alvares GA, Quintana DS, Hickie IB, Guastella AJ. Autonomic nervous system dysfunction in psychiatric disorders and the impact of psychotropic medications: a systematic review and meta-analysis. J Psychi & Neurosci. 2016; 41(2):89–104. doi: 10.1503/jpn.140217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Friedman BH, Thayer JF. Autonomic balance revisited: panic anxiety and heart rate variability. J Psychosomatic Res. 1998;44(1):133–151. doi: 10.1016/S0022-3999(97)00202-X. [DOI] [PubMed] [Google Scholar]
- 41.Healey JA, Picard RW. Detecting stress during real-world driving tasks using physiological sensors. IEEE Trans Intel Trans Systems. 2005;6(2):156–166. doi: 10.1109/tits.2005.848368. [DOI] [Google Scholar]
- 42.Kreibig SD. Autonomic nervous system activity in emotion: A review. Bio Psych. 2010;84(3):394–421. doi: 10.1016/j.biopsycho.2010.03.010. [DOI] [PubMed] [Google Scholar]
- 43.Brook RD, Julius S. Autonomic imbalance, hypertension, and cardiovascular risk. Am J Hyperten 2000;13(S4):112S–122S. doi: 10.1016/S0895-7061(00)00228-4. [DOI] [PubMed] [Google Scholar]
- 44.Carnethon MR, Golden SH, Folsom AR, Haskell W, Liao D. Prospective investigation of autonomic nervous system function and the development of type 2 diabetes: the Atherosclerosis Risk In Communities study, 1987–1998. Circulation. 2003;107(17):2190–2195. doi: 10.1161/01.CIR.0000066324.74807.95. [DOI] [PubMed] [Google Scholar]
- 45.Malik M Heart rate variability. Annals of Noninvasive Electrocardiology. 1996;1(2):151–181. doi: 10.1111/j.1542-474X.1996.tb00275.x. [DOI] [Google Scholar]
- 46.Kemp AH, Quintana DS. The relationship between mental and physical health: insights from the study of heart rate variability. Int. J Psychophys 2013;89(3):288–296. doi: 10.1016/j.ijpsycho.2013.06.018. [DOI] [PubMed] [Google Scholar]
- 47.Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Reviews. 2008;12(3):197–210. doi: 10.1016/j.smrv.2007.07.007. [DOI] [PubMed] [Google Scholar]
- 48.Malliani A, Pagani M, Montano N, Mela GS. Sympathovagal balance: a reappraisal. Circulation. 1998;98(23):2640–2643. doi: 10.1161/01.CIR.98.23.2640. PMID: 9843477. [DOI] [PubMed] [Google Scholar]
- 49.Montano N, Porta A, Cogliati C, Costantino G, Tobaldini E, Casali KR, Iellamo F. Heart rate variability explored in the frequency domain: a tool to investigate the link between heart and behavior. Neurosci & Biobehav Reviews. 2009;33(2):71–80. doi: 10.1016/j.neubiorev.2008.07.006. [DOI] [PubMed] [Google Scholar]
- 50.Peschel SK, Feeling NR, Vögele C, Kaess M, Thayer JF, Koenig J . A Meta‐analysis on Resting State High‐frequency Heart Rate Variability in Bulimia Nervosa. Euro Eating Disorders Review. 2016;24(5):355–65. doi: 10.1002/erv.2454. [DOI] [PubMed] [Google Scholar]
- 51.Burton AR, Rahman K, Kadota Y, Lloyd A, Vollmer-Conna U. Reduced heart rate variability predicts poor sleep quality in a case-control study of chronic fatigue syndrome. Exp Brain Res. 2010;204(1):71–78. doi: 10.1007/s00221-010-2296-1. PMID:20502886. [DOI] [PubMed] [Google Scholar]
- 52.Mullington JM, Haack M, Toth M, Serrador JM, Meier-Ewert HK. Cardiovascular, inflammatory, and metabolic consequences of sleep deprivation. Progr in Cardiovasc Diseases. 2009;51(4):294–302. doi: 10.1016/j.pcad.2008.10.003. PMID:19110131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Bradley TD, Floras JS. Obstructive sleep apnoea and its cardiovascular consequences. The Lancet. 2009;373(9657):82–93. doi: 10.1016/S0140-6736(08)61622-0. [DOI] [PubMed] [Google Scholar]
- 54.Vail-Smith K, Felts WM, Becker C. Relationship between sleep quality and health risk behaviors in undergraduate college students. Coll Student J. 2009;43(3):924–930. [Google Scholar]
- 55.Misra R, McKean M. College students’ academic stress and its relation to their anxiety, time management, and leisure satisfaction. Am J Health Studies. 2000;16(1):41–51. [Google Scholar]
- 56.Oliver MD, Datta S, Baldwin DR. Wellness among African-American and Caucasian students attending a predominantly White institution. J Health Psych 2017:1359105317694484. doi: 10.1177/1359105317694484. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Gaultney JF. The prevalence of sleep disorders in college students: impact on academic performance. J Am Coll Health. 2010;59(2):91–97. doi: 10.1080/07448481.2010.483708. [DOI] [PubMed] [Google Scholar]
- 58.Akman T, Yavuzsent T, Sevgen Z, Ellidokuz H, Yilmaz AU. Evaluation of sleep disorders in cancer patients based on Pittsburgh Sleep Quality Index. Euro J Cancer Care. 2015;24(4):553–559. doi: 10.1111/ecc.12296. PMID:25727241. [DOI] [PubMed] [Google Scholar]
- 59.Baroni A, Bruzzese JM, DiBartolo CA, Ciarleglio A, Shatkin JP. Impact of a sleep course on sleep, mood and anxiety symptoms in college students: A pilot study. J Am Coll Health. 2018;66(1):41–50. doi: 10.1080/07448481.2017.1369091. [DOI] [PubMed] [Google Scholar]
- 60.Van Cauter E, Spiegel K, Tasali E, Leproult R. Metabolic consequences of sleep and sleep loss. Sleep Med. 2008;9:S23–S28. doi: 10.1016/S1389-9457(08)70013-3. PMID:18929315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Kloss JD, Nash CO, Walsh CM, Culnan E, Horsey S, Sexton-Radek K. A “sleep 101” program for college students improves sleep hygiene knowledge and reduces maladaptive beliefs about sleep. Behav. Med. 2016;42(1):48–56. doi: 10.1080/08964289.2014.969186. PMID:25268924. [DOI] [PubMed] [Google Scholar]
- 62.Blake MJ, Sheeber LB, Youssef GJ, Raniti MB, Allen NB. Systematic review and meta-analysis of adolescent cognitive–behavioral sleep interventions. Clin. Child and Family Psych Rev. 2017;20(3):227–249. doi: 10.1007/s10567-017-0234-5. PMID:28331991. [DOI] [PubMed] [Google Scholar]
- 63.Irish LA, Kline CE, Gunn HE, Buysse DJ, Hall MH. The role of sleep hygiene in promoting public health: A review of empirical evidence. Sleep Med Rev 2015;22:23–36. doi: 10.1016/j.smrv.2014.10.001. PMID:25454674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Levenson JC, Miller E, Hafer BL, Reidell MF, Buysse DJ, Franzen PL. Pilot study of a sleep health promotion program for college students. Sleep Health. 2016;2(2):167–174. doi: 10.1016/j.sleh.2016.03.006. PMID:27525300. [DOI] [PMC free article] [PubMed] [Google Scholar]


