Part 1 Sleep Stats and General Information Sleep is not just a rest for our brain and body but is absolutely essential to our health and function. Sleep deprivation has similar effects of alcohol on how our brain and body functions and, if prolonged enough, can actually result in death. 50-70 million Americans report a sleep disorder, with 25 million of those reporting obstructive sleep apnea (Institute of Medicine, 2006). While individual needs may vary, sleep stats reveal more and it is generally accepted that adults require 7-9h of sleep per 24h period (National Sleep Foundation, 2010). A reported 35% of adults in the US report less than 7 hours/night of sleep, and 28% report frequent insufficient sleep (Institute of Medicine, 2006).
Effects of Sleep Deprivation The acute effects of sleep deprivation include impaired mental and physical function (figure 1.). The changes in concentration and efficacy that you probably notice when you don’t get a good night’s sleep. In addition to these functional effects that we are aware of, a number of other processes occur during sleep that are important to our overall health, including immune function regulation, hormone secretions responsible for growth, repair, even appetite. Chronic and cumulative sleep deprivation, defined as less than 7h/night for morethan 14 days 1
out of 30 (Institute of Medicine, 2006), are associated with increased risk of illnesses including cardiovascular disease, diabetes, obesity, and depression (Buxton & Marcelli, 2010; Strine & Chapman, 2005). In fact, 3-5% of obesity can be attributed to sleep insufficiency (Buxton & Marcelli, 2010) – and while that may seem insignificant, consider that that is independent of any dietary, physical activity, or other metabolically related variable.
CDC Morbidity and Mortality weekly report 60(8); 2011.
The Importance of Sleep Why is sleep so important? Are its benefits just a function of allowing our brains and bodies much needed respite from the activities and demands of the day? Or is it an active process in and of itself? There’s a reason that our body wants to sleep when it’s dark and wake when it’s light, which have to do with circadian rhythms and hormone release. Many of the hormones responsible for processes from metabolism and appetite to cellular growth and repair are released from the brain in a cyclic pattern that follows that of the sun – our circadian rhythms. When sleep is cut short or not paired with environmental light/dark cycles, this can wreak havoc on the processes that those hormones regulate. Sleep deficiencies and disorders may therefore contribute to obesity, impaired immune function and infection, wound or injury healing, in 2
addition to the many other functions that a rested brain and body are required for.
Not All Sleep Is Created Equal Further, not all sleep is created equal. Different types of sleep, as indicated by different types of brain waves measured on an EEG, play different roles in rest, repair, and function of the body and the brain. The timing of these types of sleep are important and contribute to our overall quality of sleep – are we resting and repairing to optimize function? For example, slow wave sleep (SWS) happens more in the first half of the night. SWS is critical for the release of hormones, as well as for clearing wastes of the brain cells themselves. Brain cells don’t have blood supply like the rest of the body’s cells. Thus, the removal of wastes is less constant during wakefulness. Our brain is only 2% of our body mass but uses up to 25% of our daily energy – so it’s swinging well above its weight class. But with energy use comes by-products and wastes of metabolism, that can impair brain function (consider how snappy and clear your brain is at the end of a long day – i.e. neither snappy, nor clear.). During SWS, brain cells can shrink up to 60%. This allows the cerebral spinal fluid that the brain sits in to wash over cells, and clears metabolic wastes the accumulate throughout the day. This process is essential for mental function including concentration, memory formation, problem solving, and creativity. It also helps with coping with stress and emotional regulation.
Sleep and Exercise During the latter half of the night, REM sleep is more common. This is when dreams happen but also when short term memories learned throughout the day are converted into long-term memory. Neural networks are formed allowing you to consolidate the information taken in during the day. If you’ve ever found yourself dreaming about the things you were working on that day, this is a clear example of how your brain is anything but off when you’re asleep. This series will explore the relationship between sleep and health. Furthermore, it will explore how exercise affects health through changes in sleep quality as an active process.
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Part 2
Sleep Physiology What Makes Us Fall Asleep? This is an important question because if we know what factors contribute to our drive to sleep the we can know how to get better sleep. Our inclination to sleep is not as simple as it seems. There are multiple driving factors relating to both circadian rhythms of the body and metabolic factors. Metabolic fatigue in your brain, sleep physiology, and its drive to make you want to sleep increases with number of hours awake. Basically, when your brain is on, it uses energy and the process of using energy creates wastes that slow thinking and make you sleepy. The more energy your brain has expended thinking, problem solving, dealing with stress, the more wastes build up, the more tired you feel (Lorenzo 1995). This is a big contributing factor to feeling sleep initially – thinking is harder and your eyes feel heavy. Although this might be what drives you to put your jammies on, it’s actually the circadian rhythms of your body that will keep you asleep and determine the quality of your sleep.
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Fluctuations and Sleep Physiology Circadian rhythm drivers of sleep include melatonin and body temperature. Most people don’t realize that your body temperature fluctuates throughout the day and it’s a very important factor in your sleep quality. It’s like what happens during hibernation. Essentially our body temperature dips until about 6am. The lower body temperature promotes slow wave sleep. This is critical for clearing wastes from your brain promoting cognitive function the next day (Lazar et al. 2015). Getting enough hours before 6am is critical for getting enough slow wave sleep for optimal brain function – 6-8 hours before 6am is ideal (that means getting to sleep before midnight). As you get older the core temperature fluctuations change such that your body temperature rises earlier in the night – this is why older people tend to wake up earlier and why some older people have a hard time getting restful sleep, as slow wave sleep is impaired (Dijk et al. 2000).
Fluctuation of Melatonin Lastly, the daily fluctuation of melatonin is one of them most important factors in our sleep timing and quality. It is released from the brain in a way that follows the pattern of the sun rising and setting because its release is inhibited by light. This means that it is low during the day when the sun is up, and higher at night when the sun sets. It also means that our habits and dependence on artificial light can interfere with melatonin production, impairing sleep onset and quality (Lazar et al. 2015). This is extremely important because melatonin promotes the release of anabolic hormones (building and repair hormones). Furthermore it is an anti-oxidant, and inhibits inflammation and catabolic hormones. For this reason, it’s critical for maintaining a healthy body and is especially important in growing bodies and a body in repair (i.e. post-injury, post-surgery, post-exercise). It’s also important for the formation of new neural networks that turn short-term memories into long-term memories (i.e. learning). The long and short of it is that melatonin is very important for sleep quality and the effects that our sleep habits have on our physical and mental health and function.
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Measuring Sleep Patterns Sleep phases are generally evaluated by polysomnography – a combination of brain activity, eye movement, and muscle activity. Brain activity is measured by wavelength using encephalography (EEG), while eye movement and muscle activation are measured by electroculography (EOG) and electromyography (EMG), respectively. Using these measures, sleep can be characterized as rapid eye movement sleep (REM) or non-rapid eye movement sleep (NREM). NREM is further separated into stages 1-4, with 1 being very light sleep and 3-4 being very deep sleep – the respective characteristics are given in greater detail in figure 1.
Figure 1. Characteristics of REM and NREM stages 1-4 sleep by EEG, EMG, and EOG.
Notable Phases of Sleep REM sleep – REM occurs perfominantly in the end of the night, and is characterized by high activity on EOG and EEG, and very low activity on EMG. It is critical for learning and memory consolidation and is sensitive to melatonin concentrations. A common concern among sleep scientists and medical professional is the effect of electronics on REM sleep. Blue light from electronics suppresses melatonin released from the brain, which is thought to impair REM sleep quality and therefore may effect learning. 6
Melatonin also inhibits cortisol release, so these hormones fluctuate throughout the day/night inversely (when melatonin is high, cortisol is low and vice versa) (Reidner et al. 2007). This is important because cortisol is a stress hormone and, while it has some important functions, if it is allowed to stay high all the time, it can contribute to the development fo stress related illness. It’s also why sleep is extra important during times of stress.
REM Sleep is Critical During Periods of Learning and Training Slow Wave Sleep – SWS is restorative and important for promoting rest and recovery of your brain and your vital organs. Our organs are controlled by our involuntary autonomic nervous system. This system has two arms: the sympathetic system is activating, while the parasympathetic system is relaxing. SWS decreases sympathetic activity. This allows our vital organs to rest and recover (they are on all day, after all!). SWS is also critical for brain recovery and clearing wastes to promote optimal cognitive function in the morning. SWS is Critical When Next day Performance is Important.
Figure 2A – Proportion of time during sleep that is spent in the respective phases of sleep. Figure 2B – The timing of respective sleep phases. More time is spent in slow wave sleep at the beginning of the night. In contrast, REM sleep occurs predominantly towards the end of the night.
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Part 3
Sleep and Health We know that sleep is important for functioning and feeling energetic, but it is also an active contributor to our overall health. Our sleep and health are related! Hormones released during sleep decrease inflammation, fight free radicals, activate our immune system, and help organs rest and repair to keep them healthy and functional. The central effect of sleep in maintaining health is in the imperative role it plays in maintaining a balance between our various stress systems. The HPA axis (cortisol), the autonomic nervous system (fight or flight responses), and inflammation are all impacted. These systems are activated to deal with day to day stressors and must be kept in balance to maintain health (see figure 1). When they’re turned on too high, they cause wear and tear on our organs, making us feel stressed and anxious. However, when they aren’t responsive, we can underreact to situations that require us to be vigilant.
This section of the Sleep Series will discuss the effects of sleep on brain health and function, cardiovascular health and weight management, and immune function.
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Brain Health and Function The impact sleep has on how we function is most obviously experienced in how our brain works. When we get a great sleep, we’re sharp, focused, productive, and can solve any problem with creativity and perseverance. When we don’t get enough sleep, we’re slow, distracted, irritable, and have a hard time staying on task, especially if that task proves challenging. The reasons for this lie in the important active processes of sleep. Namely, these are the removal of metabolic wastes during slow wave sleep, the formation of neuronal connections during REM sleep, and the release of hormones that keep inflammation and other stress hormones low.
Metabolic Waste Clearance All animals require sleep, so it must be vital, but why is it so critical to life? An incredible study by Xie et al. in 2012 used photon-imaging in mice to uncover the mystery of sleep. They studied mice in waking states and sleeping or anesthetized states and found that the interstitial space around brain cells expands by 60%, which allows a greater exchange of wastes from within the cell with the cerebrospinal fluid moving around the cell. Basically, you can think of the brain cells shrinking to allow cerebrospinal fluid to wash over the brain cells, clearing them of wastes. The waste product in question is called amyloid beta, which builds up in brains cells that are producing/using a high degree of metabolic energy (i.e. cells that are working hard). This build up interferes with the effective and efficient function of these cells, slowing conduction of neural transmission, thereby requiring more energy to be made for the same brain functions to occur. And hence, your brain doesn’t work so good. These amyloid beta proteins have also been implicated in the development and progression of cognitive decline during old age, including dementia and Alzheimer’s .
Sleep VS Awake Figure 1. B. Shows the amount of area covered by cerebrospinal fluid (CSF) when asleep (green) compared with awake (yellow). C. Shows this same observation by percentage of area of the brain covered. This illustrates that more than 65% of the brain is covered during sleep, compared to less than 5% during wakefulness. This means that ~60% more volume of the brain is exposed to CSF, allowing the wastes to be removed from those cells. Xie et al; 2012.
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Formation of Neural Connections During REM sleep, the process of memory consolidation occurs, turning short-term memories formed during the day into long-term memories to be stored for the future. P-waves released from your pons (brain stem) during REM sleep activate your amygdala and hippocampus, which solidify memories (Datta et al. 2004). This is critical for learning processes to occur – when rats taught a maze pathway had REM sleep interfered with, they continued to struggle with the maze, while those who were allowed REM sleep undisturbed learned the path effectively (Datta et al. 2004). This goes for all kinds of learning: academic (hello, teenagers? Come in, teenagers?), occupational, sports – you name it, REM sleep is involved in remembering something that you know today, tomorrow. Figure 2. P-waves projected from the pons to the hippocampus and amygdala during REM sleep. These promote the formation of neural connections and memory consolidation that underlie the brain processes of learning.
Energy Repletion & Hormone Stabilization Partial sleep deprivation is associated with reduced cerebral metabolism in the prefrontal and cortical brain regions (Kahn-Greene et al. 2007). These regions are critical for executive functions including goal setting, attention, focus, cognitive flexibility, and working memory. This seems like a lot of functions, and it is. Further, these functions are needed for everything from solving a problem at work, to sticking to deadlines, to coping with emotional stress, and eating vegetables for dinner instead of chips and wine (what? No, I didn’t). Our ability to make good decisions relies on good executive function, so when there’s no fuel in the tank or when those parts of the brain are fatigued, we’re more likely to make bad decisions or quit when the going gets tough. In the long term, this can have lasting effects because the brain’s structure and function is determined by a “use it or lose it” principle. Effectively, if we’re too tired to make good decisions, problem solve, regulate our emotions, etc. such that we are flexing these functions less and less, the brain networks that underlie those functions start to get rusty and become more difficult to activate. Ultimately, we become our sleepiness-induced bad habits. Brain scans of people 10
with chronic partial sleep or sleep disorders like sleep apnea show long-term restructuring of the brain – a long-term sleep deprivation maladaptation (Canessa et al. 2010). When our stress regulatory brain regions don’t work well or the neural pathways that regulate stress become overgrown, our body is more likely to stay in fight or flight mode, which has lasting health consequences.
Quick Facts Brain function after acute partial sleep deprivation (<6h/night for days): • Lower Attention • Reduced Cognitive Performance • Lower Emotional Regulation • Mood Disturbance • Lower Reaction Time • Lower Motor Control & Coordination • Impaired Working Memory Brain function after chronic partial sleep deprivation (<6h/night for months – years): • Structural Brain Changes • Impaired Executive Function • Impaired Emotional Regulation • Poorer stress regulation (and associated health consequences)
Cardiovascular and Metabolic Health Sleep doesn’t just make us feel rested but is actually considered by epidemiologists (people who study population trends in illnesses) to be a health imperative (Luyster et al. 2012). Everyone knows that being physically active is good for your cardiovascular health and helps promote a healthy body weight. So, it may be counter-intuitive to discover that sleep – basically the opposite state of physical activity – is also good for your cardiovascular health and body weight. There is, of course limits to this. It’s not just “more sleep = more health.” However, very reliable evidence exists that partial sleep deprivation increases cardiovascular risk factors like hypertension and chronic inflammation. In addition, it impairs metabolic function resulting in obesity and diabetes. 11
Cardiovascular Health A study of 5500 people reporting When insufficient sleep becomes a habit, our body will spend more time than it should in an activated state, such that our vital organs donâ&#x20AC;&#x2122;t get the rest they need. As shown in the figure below, an inverted-U pattern has been reported, in which <7h/night or >8h/night is associated with higher risk of hypertension (Luyster et al. 2012). While hypertension is an independent risk factor for cardiovascular disease, itâ&#x20AC;&#x2122;s not the only one affected by chronic sleep insufficiency. Excessive sympathetic activation results in chronic inflammation and immune stimulation, which is thought to be a significant risk factor in the development of cardiovascular disease (Faraut et al. 2012). Inflammatory signaling contributes to lasting remodeling of the heart and blood vessels, and is another risk factor in cardiovascular disease and all-cause mortality.
Figure 3. The likelihood of having hypertension according to average number of hours of sleep per night. Luyster et al.; 2012.
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Obesity & Metabolic Function A single night of partial sleep deprivation will make you inclined to eat more (Brondel et al. 2010). As shown in figure 4, an inverted-U relationship between both BMI (Taheri et al. 2004) and type II diabetes (Gotlieb & Punjabi, 2005) incidence exists for number of hours of sleep per night, similar to that for hypertension shown in figure 3. The astute reader may say, “well of course you’ll eat more – you’re awake for more hours, and therefore you will consume more calories.” However, a reader remembering that decision making is impaired may say, “no, your willpower is reduced, so you have lower self-control.” While these are both probable contributors to the effects of sleep on metabolic regulation, the regulation of appetite hormones and metabolic hormones is an active process that occurs during sleep (Spiegel et al. 2004). Specifically, the hormones that make you feel hungry increase, while the hormones that make you feel full decrease. This adds up to you feeling hungrier (on average by 24%!), in addition to having lower self-control and more hours awake with the fridge (Spiegel et al. 2004).
Fluctuations of Cortisol Other metabolic contributors to the relationship between sleep and obesity exist, including the fluctuations of cortisol. Cortisol is a stress hormones that stimulates glucose circulation in the blood and the metabolic pathways that use glucose for energy. When these are increased with no stress increasing the demand for glucose, it just stays in the blood or goes into storage mode. This is kind of like the boy who cried wolf. Eventually, the receptors that respond to cortisol, insulin, and blood glucose stop heeding the call and become less responsive. Ultimately, this leads to the dysfunctional glucose metabolism, known as insulin resistance, that underlies metabolic syndrome, type II diabetes, and obesity.
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Figure 4. Inverted-U relationship between average hours of sleep and BMI. Roughly 7.7 relates to the lowest BMI. Taheri et al.; 2004. The odds ratio (likelihood) of experiencing diabetes of impaired glucose tolerance – a test for glucose metabolic function – according to average hours of sleep. Gotlieb & Punjabi; 2005.
Immune Function Our immune system is comprised of two arms that work together: the innate immune system and the adaptive immune system. The innate system targets anything that it identifies as “non-self”, but to fight pathogens, it must randomly encounter them in the blood, or follow biomolecular signals released from another immune cell that’s already encountered the pathogen. While it has to depend on these random encounters to protect the body from would-be invaders, it has the benefit of acting immediately to neutralize the threat. Conversely, the adaptive immune system is shown the specific patterns of the pathogen in question (more specific than just “non-self”). It creates an army of these cells ready to attack. And with the “picture” of the perpetrator, go hunting in the blood/body. While this is a more effective and targeted way of taking care of invaders, it takes a little longer to build and disseminate the army of cells. The innate system has enough fire power to keep the invader at bay until the adaptive system is trained and en route. But, eventually, it will lose out to the pathogen without the adaptive system’s action, resulting in infection and illness.
Sleep and Innate Immunity During sleep deprivation, stress hormones increase (epinephrine, norepinephrine, cortisol) and anabolic hormones decrease (dopamine, prolactin, growth hormone) (Meerlo et al. 2002). Stress hormones can promote inflammatory signaling by activating NFkB, which controls inflammatory genes in the cells (Irwin et al. 2006). This is important because not only are these inflammatory markers signals for immune function, they are well-known risk factors for most chronic illnesses (cardiovascular disease, metabolic syndrome, diabetes) and mental illnesses (depression, chronic fatigue). High basal levels of inflammation also impair cognitive function, making your brain slow and foggy. Since slow wave sleep happens more predominantly in the early part of the night, staying up late to finish a paper or report or to socialize with friends is the most likely type of partial sleep deprivation to impair immune function (Irwin et al. 1994, 1996). 14
Sleep and Adaptive Immunity Melatonin, in addition to being a sleep regulating hormone, is also an anti-oxidant and immune regulator. In addition to promoting the release of growth hormone, it also scavenges free radicals and protects the cells’ mitochondria. These functions protect cells from damage, DNA dysfunction, and cell death – all of which contribute to a healthier brain and body. Interestingly, the effects of a given stressor on adaptive immunity can be seen in their response to an immunization, since an immunization is basically doing the body’s job of showing the cells the “picture” of the “perpetrator” or pathogen ahead of actually coming into contact with it in the body. The adaptive system will make an army so it is ready to fight whatever pathogen it is trained to fight (i.e., flu, polio, TB, or whatever). It does this by producing antibodies that are specific to that pathogen. The more antibody produced, the stronger the adaptive immune system response.
Marginalized Sleep Using this technique, Lange et al. 2003, show lower antibody production to Hepatitis A when participants were deprived of sleep after they got their Hep A shot (figure 5). This is because the promoting effects of melatonin on cells of the adaptive immune system is reduced, resulting in lower production of antibody, and greater likelihood of infection. It’s not surprising that studies have also shown a greater susceptibility to the common cold and respiratory tract infections (i.e. sore throat, cough) when sleep is marginalized (Wilder-Smith et al. 2013). Interestingly, when your body is fighting an infection, you tend to spend more time in slow wave sleep (Madje & Krueger, 2005). This effectively puts your body in a state of high immune function to fight the infection. It also explains why quality sleep keeps us healthy and helps us recover. Figure 5. Antibody production in response to hepatitis A vaccination. The black line indicates antibody production when immunization was followed by sleep deprivation, compared with the white control line. Lange et al.; 2003.
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Quick Tips • Don’t sacrifice early night sleep (10pm-3am). This is when you get most of your slow wave sleep and is essential for a healthy immune system. It’s better for your health to go to sleep and wake up early to complete any work from the previous night. • If you feel yourself coming down with something, prioritize early night sleep to give your immune system the time and support it needs to fight off whatever illness is trying to get you down. • Women take longer to recover from sleep deprivation – so go ahead and put your feet up or take a nap! It’s better to steal a couple hours of extra sleep than be down for the count with a flu or cold for days or even weeks.
Bringing It All Together Consequently, the effects of poor sleep habits have long-term effects on your health. This includes brain structure changes, which promote stress reactivity and illness processes related to stress. During this state, our autonomic system chronically activates and our organs that work all day don’t get the necessary time to rest, repair, and recover for the next day’s work. Hence, this can contribute to psychological illnesses (depression), cognitive illnesses (dementia), cardiovascular illnesses (hypertension), metabolic illnesses (diabetes & obesity), and immunosuppression (cancer & viral/bacterial infections). Overall, not only is your productivity and physical competency suffering, but your risk of illness and all-cause mortality (aka. “death”) increases! We’re far too quick to sacrifice sleep to make time for other things that we consider to be more important. But just because sleep doesn’t require effort, doesn’t mean it isn’t an active process that is essential for our body’s function, health, and happiness.
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Part 4 Exercise and Sleep Quality There is lots of research that shows improved sleep quality is one of the many secondary benefits of exercise, beyond those of just fitness and body composition. From children to older adults, healthy individuals to patients of all types of ailments, exercise seems to help us sleep better. This is one of the most overlooked health benefits of exercise – optimizing rest so that you’re contributing to your health even when you aren’t awake. Sleep is so important for how our brain and body feel and function. Nearly 30% of adult Americans report insufficient sleep. Sleeping pills come with adverse effects and they shouldn’t be taken on a long-term basis. That leaves exercise as one of the only long-term solutions for resolving sleep deficiencies. So, what is it about exercise that helps us sleep better and are all types of exercise created equal? Is getting a good sweat just inherently good for sleep or are the cumulative effects of exercise-induced fitness changes at the root of improved sleep quality? This section will explore the benefits of HIIT, aerobic exercise, resistance training, and low-impact exercise on sleep quality and try to uncover just how exercise helps us sleep (see figure 1.)
How Does it Work? In general, when you exercise, you improve your sleep quality that night by 17
straining your brain, decreasing your body temperature, and increasing parasympathetic drive. Physical effort takes a lot of mental work! You expend energy pushing your body when it wants to quit, and use up existing energy stores in the body, which contribute to the homeostatic drive to sleep. This helps you fall asleep earlier and promotes slow wave sleep (labeled ‘CNS fatigue’ in figure 1.). When you exercise, your body temperature increases with the metabolic effort you exert. You have a set body temperature range that your body wants to maintain where cells function the best (98.6°F; 37°C). When you take your body temperature above that range, your body makes adaptations to bring it back down, usually overshooting and dropping your body temperature lower than before you started your exercise. The lower body temperature helps you get into a deeper sleep and, like the CNS fatigue, helps promote slow wave sleep leaving you feeling well-rested in the morning. Better body temperature regulation is also one of the contributing factors to better sleep quality with regular exercise. As the insulating effects of excess subcutaneous (under the skin) fat is lost and metabolic changes promoting efficiency at the cellular level occur, heat production at rest is regulated better.
Post-Exercise Effects Similar to the reflexive overcompensation of body temperature after exercise, changes in sympathetic/parasympathetic nervous system balance have delayed post-exercise effects. During exercise, your sympathetic “fight or flight” system is activated and parasympathetic drive is reduced. This helps support exercise by increasing heart rate, blood pressure, breathing rate, and muscle activation. When you finish your exercise, the reverse happens: parasympathetic drive increases and sympathetic drive decreases. The parasympathetic switch can be observed as lower heart rate and blood pressure but it also contributes to a restorative and repair processes in the body that are less noticeable. Autonomic nervous system balance is also a contributor to long-term adaptations with increased physical fitness and one of the reasons that training programs help you sleep better on the regular. It’s also part of why athletes have low heart rates.
Central Nervous System Fatigue It’s important to note that these reflexive changes in body temperature and parasympathetic activity, and the central nervous system fatigue that contribute to 18
better sleep during the night after your exercise take some time to take effect. So, exercising within a couple hours of bedtime can actually make it harder to fall asleep. This is important when youâ&#x20AC;&#x2122;re timing your exercise, especially if youâ&#x20AC;&#x2122;re hoping to improve your sleep quality with your exercise program. Figure 1. Acute and chronic changes induce by exercise that promote sleep quality. (From Uchida et al. 2012).
1. Aerobic Training and Sleep Aerobic exercise has been long thought to improve sleep quality. The relationship between aerobic activity and sleep has come from observations that aerobically fit people fall asleep faster, have deeper sleep, and sleep longer (Edinger et al., 1993; Baekeland & Lasky, 1966). Higher self-rated sleep quality has been reported in people who also report recent increases in activity, while the reverse is seen in people who report reduced physical activity (Sherrill, Kotchou, & Quan, 1998). The rationale behind sleep improvements with increased aerobic activity are based in the effects of aerobic activity on fatigue and body temperature. The most common changes reported with increased aerobic activity are the same for those reported in aerobically fit people: increased slow wave sleep (deep sleep), total sleep time, and decreased REM sleep, as well as increased wakefulness during the day (feeling more alert).
Effects on Depression A study of 50 to 76-year-old men and women participating in a community-based moderate intensity exercise program (low-impact aerobics or brisk walking at ~60-75% of heart rate reserve) resulted in improved sleep quality measured by a sleep questionnaire (Pittsburgh Sleep Quality Index) (King et al.1997). In people reporting poor sleep associated with depression, improvements in both sleep quality and depressive symptoms were improved. While 19
both sleep and depression can independently benefit from aerobic exercise, the authors were unable to determine whether exercise improved sleep directly or whether reported improvements in sleep were a result of reduced depression (Singh et al. 1997).
I Want Results…Now! Exercise programs improving fitness seem to help sleep but what about the acute effects of aerobic exercise today on sleep quality tonight? The acute effects of exercise seem to agree very well with the chronic effects of aerobic exercise. Acute aerobic exercise increases sleep duration by ~10min decreases REM sleep and increase stage 4 slow wave sleep (the most coveted of deep sleep) by ~4 min (Driver, 2000). The duration and intensity of exercise are important factors in the effects it will have on sleep. Longer exercise (>30 minutes) and intense exercise seem to drive the greatest improvements in sleep quality (Youngsted O’Connor, & Dishman, 1997). Since exercise also has transient effects on alertness, exercise close to bedtime.
Aerobic Exercise For Sleep Although the importance of aerobic activity on sleep quality is widely reported in anecdotal reports, there are seemingly lower effects in smaller, interventional studies. The reason for this appears to be the people included in the intervention studies who may already be aerobically fit or already have high sleep quality – so called “good sleepers”. In research, this is called the “ceiling effect” where the people being studied have little room for improvement in the intended outcome of the intervention. Therefore, aerobic exercise and/or improvements in aerobic fitness are most likely to improve sleep in people who need to improve their sleep! Hence, older individuals, women, sedentary individuals, or people who report high stress and/or low levels of physical activity (Uchida et al 2012). Demographic Factors – who will benefit the most? • Women • Older individuals • Sedentary individuals • Depressed or stressed individuals 20
Exercise Factors: • Timing of exercise – should be done >3h before bed • Duration of exercise – should be >30 minutes • Intensity of exercise – should be >65% HRmax
2. High-Intensity Interval Training (HIIT) Exercise intensity is one of the acute factors influencing sleep effects after exercise, as is aerobic fitness changes. HIIT includes high-intensity bouts interspersed with active rest bouts of a lower intensity. HIIT includes not only sprint-like activities (i.e. spin class, track workouts) but also metabolic conditioning classes like Tabata workouts. This type of exercise induces significant fatigue (both mental and physical) and is extremely effective at improving aerobic fitness. Because of this, it is thought to be an effective exercise method for improving sleep quality and quantity. No studies have investigated the effects of HIIT in healthy participants. However, given the effects of HIIT on aerobic fitness, one may expect them to be similar, if not slightly greater, than those observed in traditional aerobic training regimes. In participants with co-morbidities involving sleep disturbances, such as rheumatoid arthritis and sleep apnea, the results of HIIT programs appear promising Rheumatoid arthritis and other inflammatory illnesses are commonly associated with sleep disturbances. And these are thought to exacerbate pain and symptoms of dysfunction.
Inflamation and HIIT There is a bi-directional relationship between inflammation and sleep in which inflammation disrupts sleep, while good sleep quality reduces inflammation. HIIT can independently improve sleep and inflammation, effectively improving disease-related outcomes (Loppenthin et al. 2014). HIIT in sleep apnea patients also shows promising results. After a 12-week HIIT program in obese sleep apnea patients, aerobic fitness was improved, apnea related events were reduced, and daytime sleepiness was reduced compared with controls (Karlson et al. 2013).
Timing and HIIT Takeaways As with aerobic exercise, the time of day the HIIT is performed determines its effect on sleep that night. In healthy soccer players, it was found that HIIT training done in the evening disrupted sleep while HIIT in the morning did not (Vitale et al. 2017). 21
Another interesting element of the sleep <–> HIIT relationship is the effect of sleep on quality of HIIT training. Quality sleep is needed to allow maximal mental effort for both intellectual and physical activities. Because of the high intensity required of HIIT, poor quality sleep will have negative effects on the quality of your workout, limiting the intensity that you can muster and increasing the feelings of relative exertion of the exercise (McMurray & Brown, 1984). Overall, the guidelines for HIIT and expected outcomes on sleep quality and duration are similar to those of aerobic training. Improvements in aerobic fitness, night-time fatigue, and reflexive parasympathetic activation can help you fall asleep faster, and get a longer, deeper sleep. In people with illnesses with symptoms of sleep disruptions, inflammatory status and aerobic fitness improvements (and likely parasympathetic/sympathetic system balance) can be improved by exercise, subsequently improving sleep symptoms.
3. Resistance Training HIIT and aerobic exercise have similar physiological effects on the body. Therefore, can be expected to have similar effects on sleep both acutely and chronically. But what about weight training? Traditional resistance training doesn’t impose the same metabolic demands that aerobic or HIIT training do. Nor does it elevate core temperature to the same extent. With that said, depending on your intensity, a considerable cognitive effort is required to get through the last reps of a set and autonomic balance shifts towards parasympathetic during recovery. So, there is a reasonable physiological rationale for resistance training to improve sleep quality. On the flip side, excessive weight training that causes high levels of cortisol or muscle damage and pain can interfere with sleep. And as you may know, it’s hard to get comfortable when you can’t move from your workout. Research investigating the effects of resistance training on sleep quality is more limited than for aerobic. However, it generally points towards improved sleep quality, especially in populations with poor sleep. In a group of older people with reported sleep difficulties, a 24-week resistance training program resulted in increased total strength (19%), upper body strength (52%), and sleep quality (38%) (Ferris et al. 2005). The regimen used was fairly moderate: 50% 1 rep max load was used in a circuit that included bench press, leg press, leg curls, leg extension rowing, shoulder press, and arm curls, and only took about 30 min.
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Mixing Programs for Positive Results Similarly, in older adults with depressive symptoms, a resistance training 3x per week for 10 weeks improved sleep quality, depressive symptoms, and quality of life. Statistical modeling was used to determine the predictive variables of effects found from the program. Consequently, it found improvements in strength and improvements in general depressive scores were most strongly predictive of sleep improvements (Singh 1997). No mechanistic studies have been conducted for how resistance training improves sleep, but the limited evidence shows benefits. Some studies have included mixed aerobic and strength programs with positive results (Kline et al 2011). While both aerobic, HIIT, and resistance training seem to all improve sleep, it raises the question: Is there a type of exercise that is best? An intervention study to answer this has not been yet been conducted. However, compared with power lifters, endurance athletes have higher SWS increased sleep duration and shorter sleep onset (Trinder, Mongomery, & Paxton, 1988; Trinder et al., 1985). Therefore, if you’re really keen to get a change in sleep quality from your exercise, make aerobic training your priority.
4. Low Impact Exercise As was stated at the beginning of the exercise section of the sleep series, the most likely cause for exercise’s effects on sleep are: Hot core temperature during exercise resulting in reflexively lower temperature later (cooling the body facilitates deep, slow wave sleep – kind of like hibernation). Metabolic fatigue of the brain (and body) – exercise is hard! Not just for the body but for the brain too. The mental exertion of persevering through bodily discomfort paired with the overall fatiguing effects of exercise, help drive you to fall asleep faster. This means less time tossing and turning before drifting off. Autonomic nervous system balance – Intense exercise activates the sympathetic “fight or flight” arm of the autonomic nervous system. With the Fight or flightstimulus removed (i.e. when your workout is done), the balance shifts towards turning off the activating sympathetic system, while turning on the repair and recovery parasympathetic system. Because low-intensity exercise by its very definition is not likely to cause excessive fatigue, core temperature increase, or fight or flight drive, how can I improve sleep? 23
Low-Impact Exercise and Mindfulness Low-intensity exercise like Pilates, yoga, and Tai Chi, commonly involve some level of strength and aerobic demand. However, this is generally at relatively low levels. So, it’s more likely that the combination of controlled movement, mindfulness, and deep breathing involved in these practices that drive an increase in parasympathetic activation. And this promotes rest and recovery and facilitate slow wave sleep. There is a strong body of evidence to show that these types of low-intensity exercise practices reduce anxiety, stress, and other acute psychological disturbances. These disturbances can get in the way of sleep. A study of college students undergoing a Pilates and Taiji Quan program for a semester as a mindfulness-through-movement program found improved sleep quality correlated with increases in mindfulness (Caldwell et al 2009). Consequently, this aligns with studies showing reductions in anxiety and stress reported with these types of exercises as responsible for the improvements in sleep.
Bringing It All Together The benefits of exercise on health and wellness are far-reaching and include improvements in sleep quality. Exercise can improve your sleep the night after exercise, as well as habitually with regular exercise. All types of exercise are likely to improve sleep quality. However, aerobic exercise or HIIT training seem to be the most effective. This is especially true in populations with sleep disturbances. The immediate changes that promote sleep relate to mental/physical fatigue that helps you fall asleep faster. Furthermore, reflexive decreases in body temperature and autonomic nervous system activation help you sleep deeper. We commonly associate regular physical activity with better sleep. This is likely because of reductions in inflammation, improved autonomic nervous system balance, and decreased psychological stress, anxiety, or depression. It also probably promotes adoption of healthier habits. Examples of healthier habits include cutting back on drinking or smoking (which can hinder sleep) and eating better. Overall, exercise does more than just make us “fitter.” It keeps us healthy even when we aren’t moving.
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Part 5 Exercise and Sleep Disorders 1. Sleep Apnea What Is Sleep Apnea? Sleep apnea is one of many sleep disorders and can be either obstructive (shown in figure 1) – a physical deformation of airways causing obstruction – or central, in which your brain “forgets” to send signals to your lungs to breathe. In either case, it results in you stopping breathing briefly a few times an hour during sleep. This impairs oxygen uptake in the blood and reduces the efficacy of a number of active sleep processes (immune activation, repair etc.) and impairs your ability to get into a deep sleep. Figure 1. Deformation of airways causing obstructive sleep apnea.
Overall, you’re left with the characteristics of poor sleep – poor attention and focus, lower working memory and learning, irritability and poor self-control, and 25
overall sleepiness. These functional changes relate to structural changes in the brain, especially in the hippocampus and frontal cortex (Canessa et al. 2010). Because it disturbs the important processes of sleep that are critical to maintaining good heath, it is also associated with higher risk of heart disease & stroke, diabetes & obesity, and accidents.
Who Is Affected By Sleep Apnea? Obstructive sleep apnea is defined as 5 or more events (breathing stops) per hour during the night and affects more than 25 million Americans (Institute of Medicine, 2006). Typically, youâ&#x20AC;&#x2122;ll only know if you have sleep apnea if someone tells you or if you do a sleep study, but if you feel chronically unrested you may want to investigate with your doctor. It effects more males than females, and is also more prevalent in smokers, drinkers, and people who are sedentary and/or overweight. Therefore, lifestyle factors can have a very big impact on the progression and severity of sleep apnea.
How Does Exercise Help? Often people with sleep apnea will use a Darth Vader-like CPAP machine that uses pressurized & oxygenated air to help maintain breathing and O2 levels throughout the night. These machines are cumbersome (and a bit scary looking) and inconvenient, and may not treat the underlying cause of sleep apnea, which is thought to be related to systemic inflammation or autonomic dysregulation (Dempsey, 2010). Other lifestyle changes that improve inflammation including weight loss, smoking/drinking cessation, and exercise can help. Excess weight is a particularly impactful risk factor, so reducing excess body weight through diet and exercise can be very effective in reducing sleep apnea symptoms. Exercise also promotes an autonomic shift and anti-inflammatory effect, which likely contribute to its effect on sleep apnea.
Research/Evidence Like many other conditions for which exercise is a sort of treatment, some of the evidence comes from epidemiological self-reports, which have found that people who are physically active have a lower risk of sleep apnea (Kline et al. 2011). Exercise participation (150min/week) is associated with lower AHI events per night, the scale used to measure apnea severity. Further, sleep quality and blood 26
oxygenation have been found to be related to changes in physical fitness (Kline et al. 2011). Exercise independently improves many of the cognitive and structural changes that are characteristic of sleep apnea, as it is known to promote hippocampal growth and function (Erickson et al. 2010), learning and memory (Deng, Aimone, & Gage 2010), executive functioning, and mood/self-regulatory processes (Goldin et al. 2013). A more detailed description of exercise and sleep apnea can be found in the article here.
2. Insomnia What Is Insomnia? Insomnia is a well-known affliction that refers to significant loss of sleep –either getting to sleep or staying asleep, or non-restorative sleep. It results in loss of function during the day and other negative consequences of impaired sleep (mental/physical health, performance, cognitive function, mood emotional regulation etc.). There is no explicit cure for insomnia, so sleep habits and/or lifestyle changes are the first line of defence for improving insomnia episodes. As its origin is largely psychological, it is often the result of other underlying conditions like stress, depression/ anxiety, chronic pain, etc. or lifestyle habits like alcohol, caffeine, or smoking. However, in some cases it is considered “primary” insomnia with no Figure 2. Complications of Insomnia. underlying causes.
Who Is Affected By Insomnia? Insomnia affects about 10-15% of adults and is more common in females than males, and in older people compared to younger. About 6% of the population experiences insomnia that is not related to some underlying cause of sleep disturbance (primary insomnia). In addition to consistent sleep loss (>3 nights/ week for >3 months), dysfunction to social, occupational, educational, academic, or behavioral ability is also required for a clinical psychiatric diagnosis of insomnia. 27
How Does Exercise Help? Sleep aides (i.e. pills) can be addictive or lose efficacy over time. They can only be used as a band-aid solution. One characteristic of people suffering from insomnia is increased urinary cortisol and catecholamines (HPA/SNS activation) and higher brain and body energy use (especially glucose). Overall, this points to chronic and excessive arousal of both the brain and body’s systems. This makes it difficult to turn them down enough to get effective rest (deep sleep). This can possibly result from altered neurotransmitter populations, specifically GABA an important inhibitory neurotransmitter. Ultimately, it results in a cycle in which you can’t sleep, which impairs your body and brains ability to fully relax and repair, which causes greater activation of your body further worsening sleep issues and so on. Exercise can help promote the shift towards relaxation interrupting this dysfunction sleep cycle and starting you on a path to better sleep.
Research/Evidence Exercise early in the day helps decrease stress and psychological influences of insomnia. This happens because of a shift in the autonomic nervous system balance towards parasympathetic activity. This decreases basal activation of fight/ flight signaling molecules (catecholamines and cortisol). Furthermore, it normalizes GABA concentration and activity in the brain. Overall, it means your body’s baseline is more relaxed. Acute exercise (i.e. exercise this morning) can improve insomnia so long as the timing is not close to bed time, given the physiologically arousing effects of exercise. Moderate intensity aerobic exercise seems to be better than resistance training and aerobic combined, or high-intensity exercise for alleviating the severity of insomnia symptoms (Passos et al. 2010). Exercise training programs have also shown great improvements in insomnia symptoms, regardless of time of day exercise is done (slightly different than the results of one-off exercise bouts and insomnia symptoms). Participants (~45 years old) in an exercise trial fell asleep in ~8 min compared with 17 min, woke up in the night for 40 minutes compared with over an hour, improved sleep quality from 41% to 60%, and felt significantly better rested in the morning (Passos et al. 2011). Similar findings have also been found in older individuals with chronic insomnia (>55 years old) (Reid et al. 2010). These findings suggest improvements in sleep are related to improvements in psychological functioning. 28
3. Bruxism What Is Bruxism? Bruxism essentially refers to teeth grinding or jaw clenching during sleep. Hence, symptoms tend to be worse during the day (headaches, tooth soreness) but the cause is clenching/grinding at night. However, often you don’t notice it but you carry a lot of tension in your jaw muscles. Ultimately, this can result in dental issues (sensitive/filed down teeth), tension headaches, or jaw issues. Figure 3. Jaw muscle activation leading to one of many sleep disorders: bruxism.
Who Is Affected By Bruxism? 70% of the underlying cause of bruxism relates to stress and seems to be worse for people who sleep on their back. Usually during sleep, because the paralysis of skeletal muscles that occurs, the voluntary muscles of the jaw are inactive and the jaw relaxes and opens slightly. Over-arousal of muscles – possibly because of neurotransmitters, or heightened sympathetic activation – causes clenching or grinding of the jaw. There are no real demographic risks for bruxism but people at risk of physiological stress – i.e. people with anxiety, low levels of physical activity, high stress occupational or personal lives – may have a higher risk.
How Does Exercise Help? Aides for bruxism include mouth guards, pharmaceuticals to treat the possible underlying neurological causes, psychosocial stress coping, and muscle relaxants/ paralyzers (Botox). In general, the treatment either has to protect the teeth, relax the jaw muscles, or treat the underlying stress that is causing the over-activation. And it is this over-activation that causes tensing of muscles during sleep. Exercise can promote the latter two. It reduces muscle activation with a compensatory shift from sympathetic activation to parasympathetic activation. In turn, this reduces psychological stress, anxiety, and worry. Furthermore, it reduces the somatic (body) manifestation of stress.
Research/Evidence There isn’t any peer-reviewed research investigating the effects of exercise on 29
bruxism. However, given the contribution of psychological stress to its occurrence, there’s a strong likelihood that exercise and relaxation can help manage the causes and the symptoms of it. With this in mind, the best exercise is probably aerobic or HIIT. This is because these exercises have strong anti-stress and anti-anxiety effects. Also, yoga/mindfulness practices can help promote better control over muscle activation and reduce that baseline state of being “keyed-up” that comes with too much stress.
Figure 4. Evidence-based exercise strategies for short term (day-of) and long-term (training) effects on sleep disorders.
Parting Thoughts: We’re busy, productive, successful people. We have a lot on the go and sometimes fitting everything into a day can be challenging. For people like us, it is critical to keep the wide-ranging health and function effects of sleep in mind. Functionally, we can choose to make time to do a hundred things at 70% of our potential. Or, we can choose to do fewer things at 100% of our potential. Investing in sleep is not only investing in how your brain and body feel day to day, but how they’ll feel and function over your lifetime. Get to sleep an hour before midnight. Turn off electronics 30 minutes before bed. Exercise in the morning to promote an early night’s sleep and a deep, restorative sleep. All of this can lead us to be the best version of ourselves, without sacrificing health or sanity in the process. The saying goes “you can sleep when you’re dead.” However, it might be more accurate to say, “if you don’t sleep, you risk death”. 30
References • Institute of Medicine. Sleep disorders and sleep deprivation: an unmet public health problem. Washington, DC: National Academies Press; 2006. • Buxton OM, Marcelli E. Short and long sleep are positively associated with obesity, diabetes, hypertension, and cardiovascular disease among adults in the United States. Soc Sci Med 2010;71:1027–36. • Strine TW, Chapman DP. Associations of frequent sleep insufficiency with health-related quality of life and health behaviors. Sleep Med 2005;6:23–7. • CDC. Perceived insufficient rest or sleep among adults—United States, 2008. MMWR 2009;58:1175–9. • National Sleep Foundation. How much sleep do we really need? Washington, DC: National Sleep Foundation; 2010. • Dijk DJ, Duffy JF, Czeisler CA. (2000) Contribution of circadian physiology and sleep homeostasis to age-related changes in human sleep. Chronobiol Int., 17(3):285-311. • Lazar AS, Lazar ZI, Dijk DJ. (2015) Circadian regulation of slow waves in human sleep: Topographical aspects. Neuroimage, 116:123-34. • Lorenzo I, Ramos J, Arce C, Guevara MA, Corsi-Cabrera M. (1995) Effect of total sleep deprivation on reaction time and waking EEG activity in man. Sleep,18(5):346-54. • Riedner BA, Vyazovskiy VV, Huber R, Massimini M, Esser S, Murphy M, Tononi G. (2007) • Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep, 30(12):1643-57. • Brondel L1, Romer MA, Nougues PM, Touyarou P, Davenne D. (2010). Acute partial sleep deprivation increases food intake in healthy men. Am J Clin Nutr. 91(6):1550-9. 31
References (cont.) • Canessa N, Castronovo V, Cappa SF, Aloia MS, Marelli S, Falini A, Alemanno F, Ferini-Strambi L. (2011). Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med, 183(10):1419-26. • Datta S, Mavanji V, Ulloor J, Patterson EH. (2004). Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: a mechanism for sleep-dependent plasticity. J Neurosci. 11;24(6):1416-27. • Gottlieb DJ, Punjabi NM, Newman AB, et al. (2005). Association of sleep time with diabetes mellitus and impaired glucose tolerance. Arch Int Med, 165:863-7. • Faraut B, Boudjeltia KZ, Vanhamme L, Kerkhofs M. (2011). Immune, inflammatory and cardiovascular consequences of sleep restriction and recovery. Sleep Med Rev. • Irwin MR, Carrillo C, Olmstead R. (2010). Sleep loss activates cellular markers of inflammation: sex differences. Brain Behav Immun, 24(1):54-7. • Irwin M, Mascovich A, Gillin JC, Willoughby R, Pike J, Smith TL. (1994). Partial sleep deprivation reduces natural killer cell activity in humans. Psychosom Med, 56(6):493-8. • Irwin M, McClintick J, Costlow C, Fortner M, White J, Gillin JC. (1996). Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J, 10(5):643-53. • Irwin MR, Wang M, Campomayor CO, Collado-Hidalgo A, Cole S. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med, 166(16):1756-62. • Kahn-Greene ET, Killgore DB, Kamimori GH, Balkin TJ, Killgore WD. (2007). The effects of sleep deprivation on symptoms of psychopathology in healthy adults. Sleep Med. 8(3):215-21. • Lange T, Perras B, Fehm HL, Born J. (2003). Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom Med, 65(5):831-5. 32
References (cont.) • Luyster FS1, Strollo PJ Jr, Zee PC, Walsh JK. (2012). Sleep: A Health Imperitive. Sleep. 1;35(6):727-34. • Majde JA, Krueger JM. (2005). Links between the innate immune system and sleep. J Allergy Clin Immunol, 116(6):1188-98. • Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. (2005). Sleep loss: a novel risk factor for insulin resistance and Type 2 diabetes. J Appl Physiol, 99:2008-19. • Taheri S, Lin L, Austin D, Young T, Mignot E. (2004). Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med, 1:e62. • Wilder-Smith A1, Mustafa FB, Earnest A, Gen L, Macary PA. (2013). Impact of partial sleep deprivation on immune markers. Sleep Med, 14(10):1031-4. • Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M. (2013). Sleep drives metabolite clearance from the adult brain. Science. 342(6156):373-7. • Baekeland F, Lasky R. (1966). Exercise and sleep patterns in college athletes. Perceptual and Motor Skills, 23: 1203–1207. • Caldwell K, Harrison M, Adams M, Triplett NT. (2009). Effect of Pilates and taiji quan training on self-efficacy, sleep quality, mood, and physical performance of college students. J Bodyw Mov Ther, 13(2):155-63. • Driver HS, Taylor SR. (2000). Exercise and sleep. Sleep Med Rev, 4(4):387-402. • Edinger JD, Morey MC, Sullivan RJ, Higginbotham MB, Marsh GR, Dailey DS, McCall WV. (1993). Aerobic fitness, acute exercise and sleep in older men. Sleep 1993; 16: 351–357. • Ferris LT, Williams JS, Shen CL, O’Keefe KA, Hale KB. (2005). Resistance training improves sleep quality in older adults a pilot study. J Sports Sci Med., 4(3):354-60. 33
References (cont.) • Karlsen T, Nes BM, Tjonna AE, Engstrom M, Stoylen A, Steinshamn S. (2017). High-intensity interval training improves obstructive sleep apnoea. BMJ Open Sport Exerc Med, 2:e000155. • King AC, Oman RF, Brassington GS, Bliwise DL, Haskell WL. (1997). Moderate-intensity exercise and self-rated quality of sleep in older adults. A randomized controlled trial. JAMA, 277(1):32-7. • Kline CE, Crowley EP, Ewing GB, Burch JB, Blair SN, Durstine JL, Davis JM, & Youngstedt SD. (2011). The effect of Exercise training on obstructive sleep apnea and sleep quality: a randomized controlled trial. Sleep, 34(12):1631-1640. • Løppenthin K1, Esbensen BA, Jennum P, Østergaard M, Christensen JF, Thomsen T, Bech JS, Midtgaard J. (2014). Effect of intermittent aerobic exercise on sleep quality and sleep disturbances in patients with rheumatoid arthritis – design of a randomized controlled trial. BMC Musculoskelet Disord, 21;15:49. • McMurray RG, Brown CF. (1984). The effect of sleep loss on high intensity exercise and recovery. Aviat Space Environ Med, 55(11):1031-5. • Sherrill DL, Kotchou K, Quan SF. (1998). Association of physical activity and human sleep disorders. Arch Int Med, 158: 1894–1898. • Singh et al. (1997). A Randomized Controlled Trial of the Effect of Exercise on Sleep. Sleep, 20(2):95-101. • Trinder J, Montgomery I, Paxton SJ. (1988). The effect of exercise on sleep: the negative view. Acta Physiol Scand, 133 (Suppl. 574): 14–21. • Trinder J, Paxton SJ, Montgomery I, Fraser G. (1985). Endurance as opposed to power training: their effect on sleep. Psychophysiol, 22: 668–673. • Uchida S, Shioda K, Morita Y, Kubota C, Ganeko M, Takeda N. (2012). Exercise effects on sleep physiology. Front Neurol, 3:48. • Youngstedt SD, O’Connor PJ, Dishman RK. (1997). The effects of acute exercise on sleep: a quantitative synthesis. Sleep, 20(3):203-14. 34
References (cont.) • Canessa N, Castronovo V, Cappa SF, Aloia MS, Marelli S, Falini A, Alemanno F, Ferini-Strambi L. (2011). Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med, 183(10):1419-26. • Dempsey JA, Veasey SC, Morgan BJ & O’Donnell CP. (2010) Pathophysiology of Sleep Apnea. Physiol Rev 90(1): 47–112. • Deng W, Aimone JB, Gage FH. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning, memory? Nat Rev Neurosci, 11(5):339-50. • Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E, • Kramer AF. (2011). Exercise training increases size of hippocampus, improves memory. PNAS, 108(7):3017-22. • Goldin P, Ziv M, Jazaieri H, Hahn K, Gross JJ. (2013). MBSR vs aerobic exercise in social anxiety: fMRI of emotion regulation of negative self-beliefs. Soc Cogn Affect Neurosci, 8(1):65-72. • Kline CE, Crowley EP, Ewing GB, Burch JB, Blair SN, Durstine JL, Davis JM, & Youngstedt SD. (2011). The effect of Exercise training on obstructive sleep apnea and sleep quality: randomized controlled trial. SLEEP 34(12):1631-1640. • Reid KJ, Baron KG, Lu B, Naylor E, Wolfe L, Zee PC (2010). Aerobic exercise improves self-reported sleep, quality of life in older adults with insomnia. Sleep Med, 11(9):934-40. • Passos GS, Poyares D, Santana MG, Garbuio SA, Tufik S, Mello MT. (2010). Effect of acute physical exercise on patients with chronic primary insomnia. J Clin Sleep Med, 6(3):270-5. • Passos GS, Poyares D, Santana MG, D’Aurea CV, Youngstedt SD, Tufik S, de Mello MT. (2011). Effects of moderate aerobic exercise training on chronic primary insomnia. Sleep Med. 12(10):1018-27. 35
References (cont.) â&#x20AC;˘ Institute of Medicine. Sleep disorders and sleep deprivation: an unmet public health problem. Washington, DC: National Academies Press; 2006. â&#x20AC;˘ Vitale JA, Bonato M, Galasso L, La Torre A, Merati G, Montaruli A, Roveda E, Carandente F. (2017). Sleep quality and high intensity interval training at two different times of day: A crossover study on the influence of the chronotype in male collegiate soccer players. Chronobiol Int, 34(2):260-268.
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