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The Functions of Sleep
Oxford Handbooks Online

Yvonne Harrison
The Oxford Handbook of Sleep and Sleep Disorders
Edited by Charles M. Morin and Colin A. Espie
Print Publication Date: Mar 2012 Subject: Psychology, Clinical Psychology

Online Publication Date: Sep 2012 DOI: 10.1093/oxfordhb/9780195376203.013.0004
Abstract and Keywords
The drive for regular sleep is present in many, if not all, species and is assumed to be
under the control of homeostatic and circadian systems, developed in response to a need
to adjust to geophysical (climatic, seasonal, and environmental) features of the
environment. Given that so much study time has been invested in the assumption that to
take away the opportunity for sleep will reveal the very essence of the need for that
process, very few researchers have questioned the validity of this approach. Yet sleep
loss, for many species, is costly and stressful, and in the laboratory setting the emotional
or motivational components of cognitive deficits remain largely unmonitored. An
evolutionary approach to understanding the functions of sleep assumes that clues lie in
studying differences in how sleep has developed between species and under differing
environmental conditions. This approach has provided important insight, but there are
difficulties in making comparisons between species of widely differing physiological
makeup and complexity. Interest in the relationship between sleep and memory processes
has grown rapidly in recent years, and there is a sense that we have reached a
breakthrough in our understanding of the functions of sleep. However, while key
researchers argue that sleep is an essential state for optimal efficiency in the processing
of memory, others remain unconvinced and see sleep as, at best, favorable but not
essential to the consolidation and enhancement processes presumed to underpin memory.
Keywords: sleep, homeostatic, circadian, environmental factors, memory, emotion
Introduction
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Ask children why sleep is important and they are likely to tell you that sleep is something
they have to do every night if they are to grow into strong, healthy adults. Ask their
parents why sleep is important and their explanation is likely to be along the lines of
needing sleep for physical health, vitality, and general well-being. This assumption is
mirrored in commonly held beliefs about sleep; when asked if they would like to have
more sleep, about half of over 10,000 respondents to a recent Internet survey said they
would, but this was related to perceived stress rather than reported daytime sleepiness
(Anderson & Horne, 2008), and while Groeger et al. (2004) failed to find compelling
evidence of a substantial decline in sleep duration over recent years in the British public,
when sleep difficulties were reported these were again related to difficulties encountered
in daily life. So there is a general feeling that sleep does something important for us, and
that we need to get enough or there will be some cost, but we are not quite sure what or
why that is.
However, look to the scientific literature for an explanation of why we sleep, and the story
is not that much clearer. Despite extensive efforts over the last 100 years or so, our
understanding of the functions of sleep is far from complete. The question of why we
sleep has been approached from a number of angles; some researchers compare species
and ask how sleep has developed differently in individual animals and for what apparent
benefit. Others might look to changes in sleep patterns within the (p. 62) same species
over a lifetime, or perhaps consider the effects of abstinence from sleep in either the long
or short term. Whatever the approach, a number of questions remain central to the
debate. To what extent is sleep purely an adaptive function with little or no physiological
purpose? Is sleep a process that, although costly in time, adds something positive to the
likely survival of a species? Why is it that some animals appear to function quite well
without sleep for long periods of time and that, even in humans, the effects of sleep loss
are far from dramatic? To what extent is sleep a restorative process? What is the role of
the NREM rebound that, although not universal, is an effect common to many animals
following periods of sleep abstinence, and strong evidence in support of a homeostatic
role for sleep? What about individual roles for NREM and REM sleep, or perhaps
changing roles across the life span or different environments? In reviewing these
approaches, the aim of this chapter is to provide some insight into current theories of
how sleep has evolved over time and across species, and to ask what purpose sleep might
continue to have in modern, everyday life.
This chapter will first explore the arguments concerning the emergence of sleep
specifics, in particular the role of REM and NREM sleep, before then asking to what
extent these ideas have contributed to our current knowledge of the functions of human
sleep. Two quite different positions will be explored: The first assumes that sleep serves a
vital function in the integration of sensory input with memory structures and processing
(cf. Kavanau, 2005, 2006; Walker, 2005). The second holds that sleep performs no single,
clearly discernible vital function other than to inhibit wake and that, when the need
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arises, many species function perfectly well without some, if not all, of their normal quota
of daily sleep (Horne, 2006; Rial et al., 2007; Vertes, 2005; Vertes & Siegel 2005).
The evolution of sleep
The rationale behind an evolutionary approach to understanding sleep processes assumes

that if we understand something of the environmental and functional conditions that
determined the emergence of a particular process, such as sleep, then we can go some
way toward understanding current processes and functions more clearly (Nicolau et al.,
2000). Many researchers interested in the evolution of sleep hold the view that at some
point in the history of the planet it was inhabited by animals with no need for sleep. It
follows that something must have favored the emergence of sleep, whether biological,
environmental, or behavioral, and in doing so offered a value to that species in terms of
long-term survival that outweighed the cost of immobilization, loss of awareness, and, for
some, increased risk of predation. Kavanau (2004, 2006) suggests that this event can be
traced to the development of complex visual apparatus and the concurrent increasing
demands placed on limited neuronal circuitry. It is argued that while developments in the
properties of the visual system added immense value in terms of species survival (the
ability to process a complex visual field to a greater level of acuity, allowing for increased
speed and accuracy of motor response), this required greater volume and/or complexity
of existing neuronal structures.
In particular, animals for the first time were able to form and store memories, which
reflected the complexity of their developing sensory systems and behavioral challenges.
One solution to this emerging conflict, suggested by Kavanau (2004, 2006), is the
development of multifunctionality of neuronal systems and circuitry, in which the same
area of the brain is able to engage and contribute to more than one process, thereby
circumventing some of the difficulties of limited physical brain matter or space within the
cranium. Multifunctionality, while highly efficient, is a property that persists across many
species to this day. Kavanau’s (2004, 2005, 2006) work has proved to be very influential in
recent years. On the one hand it provides an intuitively appealing picture of the
emergence of sleep in prehistoric times as a response to the emergence of more complex
physical and cognitive attributes of a species, while also going some way toward
explaining current popular ideas about sleep function in humans, in particular the role of
sleep in the processing of memories. This is an idea that has gathered considerable
momentum over the last 10 years or so of research.
One clue as to the reasons underpinning the emergence of sleep might lie with the
distinction between REM and NREM sleep. Although early psychologists engaged in the
study of sleep deprivation, such as Patrick and Gilbert (1896), observed that sleep was
not a uniform state throughout the night, perhaps amazingly the classification of sleep
into two distinct states of NREM and REM sleep was not made until the 1950s, with the
landmark discovery of REM sleep (Aserinsky & Kleitman, 1953). We are now well
accustomed to the division of sleep, at least in land mammals, into alternating periods of
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NREM and REM cycles, with clearly (p. 63) discernible neurophysiological and
behavioral patterns of activity. In humans, these states are very different. NREM sleep is
characterized by increasing levels of slow, synchronized, high-amplitude features of the
EEG and decreased (relative to wake) blood flow in the prefrontal and parietal cortices,
thalamus, hypothalamus, basal forebrain, basal ganglia, cerebellum, anterior cingulate
cortex, precuneus, and mesiotemporal cortices (Maquet, 2000; Taber et al., 2006). During
this sleep, which, particularly later stages 3 and 4, we typically think of as deeper stages
of sleep, responsiveness to external stimuli is low and arousal less likely.
In contrast, REM sleep is a period of fast, mixed, low-amplitude EEG and increased
(relative to wake) activation of the thalamus, pons, limbic structures, and occipital cortex
but reduced (relative to wake) activity in the frontal and parietal areas (Maquet, 2000;
Taber et al, 2006). In addition, during REM we see a metabolic rate similar to wake,
increased variability of heart rate and respiration, loss of muscle tone producing an
effective flaccid paralysis, and rapid eye movements. Accounts of narrative dreams are
far more likely during this state then during NREM sleep and arousal more likely toward
the end of a period of REM sleep. A lack of uniformity amongst researchers and across
disciplines led to the use of a number of alternative descriptors for these states, including
quiet vs. active sleep, paradoxical sleep, and D-sleep. This was addressed to a great
extent by the standardized classification developed by Rechtschaffen and Kales (1968)
and since widely adopted, but some early terminology persists to this day and remains
appropriate, particularly where the criteria developed for the identification of NREM and
REM states in adult human sleep may not be generalizable. This is the case in the study
of human infants, where we are left with the distinction between quiet and active sleep,
often purely for pragmatic reasons, and based to a great extent on observable behavioral
state changes. Many researchers have also questioned whether it is reasonable to apply
these criteria when searching for evidence of different sleep states in other animals,
particularly insects and reptiles (Siegel, 2008).
Taylor et al. (2000) reminds us that within an evolutionary approach we should always
look for small changes when investigating the emergence of physiological processes, such
as sleep states. With that in mind, these authors advocate that as REM sleep is more
similar to the waking state, this is the type of sleep that is most likely to have emerged
first. There is a lack of consensus on this point, and in fact many researchers advocate
the contrary position that NREM sleep is the first to emerge. So what are the arguments
in favor of the REM-first position?
If we look to animals assumed to retain many of the features of their primitive ancestors,
then the evidence is mixed. On the one hand, from the limited study of monotremes (egg-
laying mammals), we have the often-cited example of the echidna, which appears to
experience no REM sleep at all, to the recent and contradictory finding of high levels of
REM sleep in the duck-billed platypus (Siegel et al., 1998, 1999)—more on the importance
of this finding later when returning to a discussion of Kavanau’s theory of sleep and
memory. Along similar lines, Taylor et al. (2000) point toward the unexpected finding of
REM sleep in some reptiles. Secondly, in favor of the REM-sleep-first position, we are
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asked to consider the ability to regulate internal body temperature (homeothermy), which
is known to develop later in evolutionary terms. This does not happen during REM sleep,
and so it is argued that there is no adaptive advantage to the emergence of a sleep state that
is characterized by an earlier feature, i.e., to take a backward step in terms of
sustainability. Thirdly, Nicolau et al. (2000) wonder whether the high proportion of REM
sleep in mammalian young is an expression of the recapitulation theory in which
individual early development is assumed to follow the pathway of evolutionary species
development.
While Taylor et al. (2000) come down firmly in the REM-sleep-first camp, what is the
evidence in terms of the NREM-sleep-first position? Until recently, the observation of a
lack of REM sleep in early mammalian species, such as the echidna, was considered to be
strong argument in support of this position, but this was undermined by the discovery of
large amounts of REM sleep in the platypus. To add further difficulties, there is much
controversy over the existence or otherwise of NREM sleep in reptiles (Nicolau et al.,
2000), studied largely because of the assumption that current versions retain many
properties of earlier forms.
Notwithstanding these difficulties, we might ask, assuming NREM sleep is the first to be
developed, what would be the adaptive advantage of REM sleep? Taylor et al. (2000)
identify two possibilities. Firstly, a sentinel theory of the emergence of REM sleep
suggests that during successive sleep cycles REM follows NREM to prevent a period of
deep, unresponsive unconscious by increasing arousal, but to a lesser extent than wake.
This period of increased arousal allows for the maintenance of (p. 64) neuronal integrity
and gives a boost to vital cardiac and respiratory systems that have otherwise slowed
during NREM sleep. It also allows for ease of waking from a near-wake state, rather than
the deeper NREM sleep. The difficulty for this position is that wake does occur from
NREM sleep, with few ill effects, and is known to occur in hibernating species that spend
long periods of time in NREM sleep. There is also the problem of a lack of
thermoregulation during REM sleep, which intuitively does not fit well with a view that
REM is a period of preparedness for wake. A second view, known as the dynamic
stabilization theory, is more relevant for current theories of memory processing and REM
sleep, and emphasizes the role of REM in the stimulation of neuronal synapses that might
otherwise decay or be lost. These processes are further supported by the lack of muscle
tone and effective paralysis of muscle activity, which might otherwise interfere with the
maintenance of motor and sensorimotor circuitry by placing additional demands on these
processes during sleep. The role of sleep in the maintenance of memory is intriguing and
will be returned to later. For now, it seems that many researchers have decided to adopt
the middle ground and accept that REM sleep is at least as old as NREM sleep, both
emerging in response to a need to develop an alternative state to that of continuous
wake.
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Do all animals sleep?
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If we look to the current similarities and differences across the animal kingdom, we can
reflect on the variations between and within species and the relative importance of
environment, lifestyle, and physiological influences on sleep behaviors, including the
presence or absence of NREM and REM sleep, the role of the sleep cycle length, sleep
duration, and placement. Siegel (2008) provides an extensive overview of studies to date,
pointing out that only a limited number of species within each category of animal type
have been subject to repeated, objective study, using well-established and comparable
sleep-monitoring criteria. In his view, these criteria do not generalize easily across
species. Also, in many cases, animals are observed outside their normal environments,
suggesting that we have at best insight into how animals sleep within the artificial
constraints of captivity. With this in mind, Siegel (2008) maintains that the observed
variation in sleep between species can provide valuable clues to the functions of sleep.
There is the common sense assumption that sleep is vital and so essential to all species,
and that without sleep death would follow. However, Siegel (2008) notes that some
animals never seem to sleep, some go without sleep for long periods without apparent
harm, and while rats die following extended experimentally induced sleep deprivation,
this is not the case for all species, or following all experimental protocols. As for the
suggestion that both NREM and REM sleep perform separate and essential functions, it is
also noted that some marine animals do not have REM sleep, and it remains debatable
whether reptiles, fish, and insects have REM sleep. In effect, Siegel (2008) argues, many
of the common sense assumptions we hold for sleep are unsupportable in the light of
what we know about animal sleep.
We often take for granted the assumption that sleep serves some restorative function,
but, in terms of energy efficiency, REM sleep is at least as costly as wake (Horne, 2006;
Siegel, 2008). The NREM rebound following sleep abstention, widely regarded as strong
evidence in support of a homeostatic, restorative role for sleep, is not found in migratory
birds following long periods of sleepless activity, and has yet to be found in migratory
animals, or those showing large seasonal variations in activity prompted by food
availability or reproductive behaviors. While all studies of mammals, mainly derived from
zoo studies, show REM sleep in these animals, the greatest amount in any 24-hour period
is unexpectedly found in the platypus (see above).
From what we know of fish, amphibians, or insects, Siegel (2008) concludes that there is
no consistent evidence of a homeostatic role for sleep in these species, or evidence of
REM sleep, as is the case for REM sleep in reptiles. In marine animals we have a number
of interesting examples of adaptive sleep patterns. For example, during periods on land
the fur seal exhibits cycling NREM and REM sleep in both hemispheres, but during
extended periods in water (over weeks), a unique pattern of unihemispheric sleep is
found. That is, sleep occurs in one hemisphere of the brain, coinciding with closing of the
contralateral eye and inactivity of the contralateral flipper. The seal continues to receive
incoming visual stimulus from the remaining open eye and to swim with the single flipper.
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In a similar fashion, dolphins are also found to show unilateral hemispheric sleep, but
without the corresponding asymmetry in motor activity.
Following delivery in the dolphin and killer whale, newborn infant and mother swim
continuously for 4–6 weeks without sleep. During a period of acute vulnerability, this is
believed to be an example of the (p. 65) dispensability of sleep in the face of pressing
danger. So, according to Siegel (2008), sleep is not a universal process “with the same
underlying vital function in all species,” p. 212, or even, it would seem, within the same
species across the life span.
If risk of predation following the birth of live young in dolphins and killer whales has such
a marked effect on their normal pattern of sleep behaviors, we might assume that
vulnerability of this type would influence a preference for sleep behaviors in other
species. Capellini et al. (2008) asked whether a shorter NREM to REM sleep cycle length
was related to risk of predation, proposing that a reduced cycle would allow greater
vigilance for prey animals because of increased arousability at the end of each REM
period. Along the same lines, it was also proposed that those animals with a high risk of
being eaten might adopt a polyphasic sleep style across the 24-hour period, rather than a
single episode of consolidated sleep (monophasic style). Contrary to these expectations,
data from a total of 56 mammalian species—independently rated in terms of their risk of
predation, sleep location, and number of episodes within a 24-hour period—failed to
confirm correlations between risk of predation and sleep cycle length, nor did predation
risk predict the adoption of a monophasic as opposed to polyphasic sleep style. Instead,
polyphasic sleep was found in animals small in size with short sleep cycles. Despite this,
these animals slept more in total across the 24-hour period than larger mammals with a
monophasic pattern of sleep. These authors concluded that this reflects the metabolic
constraints of small animals, with limited digestive capacity and the need to feed in small
amounts at regular intervals. In addition, it was suggested that their extended total sleep
time could be due to the increased amount of time in what is described as “transitional
sleep,” i.e., the lighter stages of NREM sleep, because of the number of sleep episodes in
total. It is implied that these stages are of less restorative value than deeper NREM sleep
and in that sense the shift toward monophasic sleep in large mammals, including humans,
has considerable adaptive value by consolidating sleep in a single extended period,
thereby reducing time spent in transitional sleep.
Interestingly, when Wehr et al. (1993) looked at extending sleep-time availability in

humans (by eliminating external distraction and alternative stimulation throughout 14-
hour nights in solitary darkness), sleep is seen to revert to a polyphasic pattern, with
increased stage 1, 2, and REM sleep, increased wake between sleep episodes, increased
total sleep time, and little consequence in terms of subjective or cognitive outcome
measures. Humans are not the only animals to show increased sleep when there is very
little else to do; baboons (Bert et al., 1975), cows, and ponies (Ruckebusche, 1976) also
sleep longer when studied in captivity compared with their free-roaming state.
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Given the diversity of sleep behaviors across species, and the apparent ability within
species to adjust timing and duration of sleep in response to external factors, it is now
useful to ask how the theoretical ideas of Kavanau (2002, 2004, 2005, 2006) on the
evolutionary development of sleep and sleep function fit with this huge degree of
variation. Kavanau (2002, 2004) argues that sleep evolved primarily to handle memory
processing, and that for prehistoric animals, since requirements for complex memory
processes were minimal if at all, there was no need for sleep. Coincident with the need
for increased memory capacity came the development and reliance on more complex
forms of visual acquisition apparatus and visual processing mechanisms. The first stage
in this long process toward the development of the modern sleep state is considered to be
the shift from a state of continuous active wake in support of a simple lifestyle of largely
reflexive behaviors of predation, evasion, and reproduction toward alternating periods of
active to restful wake. The requirement for a period of restful wake, characterized by a
slowing of the EEG frequency, most likely the first move toward the slow waves currently
found in the sleep of reptiles and NREM sleep of birds and mammals, was necessitated by
a requirement for long-term storage of basic memories. Given only limited available
processing capacity, arguably fully engaged with incoming sensory information and motor
response during active wake, the need for some period of disengagement emerged. The
key to this, according to Kavanau (2005, 2006), is the development of detailed focal vision
(DVF), allowing the extraction, processing, and storage of more information from the
visual field. During periods of active wake, animals are no longer solely preoccupied with
automatic reflexive behaviors, but show, for the first time, the capacity to learn, based on
the accumulation of experiential memories.
Restful wake, eventually to become primitive sleep and finally NREM and REM sleep,
allowed some resolution of the conflict between the need to deal with the immediate
incoming sensory information and the need to secure time for learning and memory
processes within the constraints of a very basic nervous system. The advantage of sleep
in (p. 66) terms of its substantial survival value in providing an efficient and effective use
of limited neural structures would ensure positive selection. So how does this explain the
huge variation in sleep patterns across current species and, perhaps more strikingly, the
apparent success of animals without sleep?
Fish that do not sleep, according to Kavanau (2002, 2004, 2008), including schooling fish,
tuna, and some sharks, live in environmentally impoverished, predictable conditions and
follow a lifestyle of largely automatic behaviors based on inherited or intuitive hard-wired
reflexes with little need for huge stores of learned memories. So, in spite of having good
visual function, there is little requirement for sleep due to their low memory needs, as
processing conflict does not arise. In contrast, fish and other marine species with
different environmental challenges sleep for the reasons outlined above. Similarly, some
animals without vision, such as the genetically blind cave bat, do not sleep, presumably
because they do not have the heavy processing demands of relatively huge amounts of
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visual input found in most other species, or even in a closely related species of bat that,
under different environmental conditions, retained their vision (Kavanau, 2006).
An important aspect of Kavanau’s argument (2005, 2006) proposes a separation between

the functions of NREM and REM sleep, again emphasizing their role in memory
processes. This division is used to explain the lack of one sleep state or the other both
between and within species. NREM sleep is described as necessary for the reinforcement
of uncoordinated memory, whereas REM sleep deals with coordinated memory
reinforcement, principally the reinforcement of motor circuitry, hence the need for loss of
muscle tone, without which motor circuits would be engaged in the unnecessary
distraction of processing movement during this sleep state. The effect of this unwanted
muscle activity would be to reduce overall efficiency of the memory process, one of the
main factors in necessitating the need for sleep in the first place.
So why do some animals manage perfectly well without REM sleep? It is argued that the
lack of evidence for REM sleep in dolphins, porpoise, and white whales is due to the fact
that they are in constant motion and so there is no need for reinforcement of visual and
motor circuits. As noted, they have a unihemispheric form of NREM sleep and,
apparently, excellent memories, so the need for REM sleep is low. The same is argued to
be true of some birds thought to have unihemispheric NREM sleep during flight.
Consistent with this point is the finding that birds engaged in more flight time have less
REM sleep, whereas flightless birds, such as penguins, have more REM sleep.
The extent to which environmental factors govern differences in sleep patterns within the
same species was recently illustrated by Kavanau (2006) when discussing the data from a
telemetric study of jellyfish (cubomedusae jellyfish—C. flickeri) swimming freely in their
natural environment and shown to sleep for up to 15 out of 24 hours. Consistent with
previous arguments, the need for excessive amounts of sleep is believed to be due to the
fact that this type of jellyfish has multiple pairs of eyes of a similar complex design to
vertebrate eyes and that their predatory eating behaviors rely on the surveillance of a
challenging visual field and an extremely fast motor response. Sleep is seen to be an
essential response to the processing demands of this highly sophisticated visual
apparatus on a comparatively simple nervous system. However, when observed in
captivity, with ready access to essential food supplies, this same jellyfish has a greatly
reduced need for sleep.
This is claimed to be the only known example where the need for sleep within a species is
determined solely by their environmental conditions (Kavanau, 2006), yet very few
species are studied in contrasting environments. When they are, as with the limited zoo
versus free-range animal studies, we see a shift toward more sleep (not less) in certain
mammals (Bert et al., 1975; Ruckebusche, 1976). We might even include humans in this
category who, under conditions of very little stimulation or alternative to sleep, are often
observed to extend their sleep beyond normal parameters (Wehr et al., 1993; Roehrs et
al., 1989, 1994; Harrison & Horne, 1996). We also see something of this in sharks, where
one type might inhabit an environment requiring low processing needs and therefore no
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sleep (open seas) and another might live more in-shore, having a greater need for long-
term memory storage of local reference points and complex feeding styles, so they do
sleep (Kavanau, 2005).
To Summarize This Position
1. Kavanau (2005, 2006) emphasizes the importance of the relationship between

sleep and visual processes. Firstly, it is pointed out that all sleeping animals aim to
reduce visual input by closing their eyes and choosing a suitable location with
minimal visual distraction (while also benefiting from the earlier adaptation from
(p. 67) transparent to opaque eyelids). Furthermore, relative to other senses, vision
requires a huge amount of processing capacity, even without directed attention. In
some birds and marine animals, sleep is instantaneous for half of the brain on closing
of the eyes. Secondly, he makes the case that only animals with the capacity for
detailed focal vision (including vertebrates and invertebrates) sleep. Animals with no
vision do not sleep, presumably because there is no conflict in processing demands
between huge amounts of visual incoming data and memory, e.g., genetically blind
cave fish. On the other hand, the absence of sleep in animals with detailed focal
vision (see above) can sometimes be explained in terms of their lifestyle, i.e., lack of
behaviorally challenging environment.
2. Theories relating to the evolutionary development of sleep continue to be highly
influential in guiding current research into the specifics of the relationship between
sleep and memory. Both NREM and REM sleep are thought to be periods associated
with the enhancement of memories, although there are many difficulties in modeling
“memory” as a cognitive process, with much resulting inconsistency in this
literature. Some species have no need for REM sleep, and others, such as humans,
manage well without REM sleep for long periods of time. It is argued that this is due
to the highly adaptive nature of brain processes that allow the more primitive
memory functions of NREM sleep to effectively, if less efficiently, complete the task
of memory processing. This might explain the lack of memory deficit despite long-
term use of REM-suppressant drugs, such as MAOI inhibitors or antidepressant
tricyclics, or the preservation of memory during extraordinarily lengthy periods of
sleep (encephalitis lethargica) (Kavanau, 2005). Note, however, that some
researchers have taken this argument a step further by suggesting that these
processes might also be covered perfectly adequately during the waking state,
thereby negating the role of sleep as essential in this regard (Vertes, 2005; Rial et al.,
2007; Vertes & Siegel, 2005); more below. It is now time to look at the sleep-
dependent memory hypothesis in further detail.
Current focus on sleep and memory
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Since the mid-1990s, we have experienced a renewed interest in the field of sleep and
memory research, which is in part due to technological advances enabling the study of
neuroanatomical features of brain activation during sleep (Maquet, 2000; Taber et al.,
2006) and following sleep deprivation (Drummond et al., 2000, 2001; Thomas et al., 2000),
but also coincident with the appealing evidence from evolutionary and comparative
studies outlined above. The extent to which sleep is implicated in memory function is so
compelling for some researchers that it has been argued that, in humans, some aspects of
visual memory can occur only during sleep (Gais et al., 2000; Stickgold et al., 2000).
However, despite the vast number of study hours devoted to this subject in recent years,
this field is marked by inconsistencies and failure to provide conclusive evidence of the
precise nature of the link between sleep and memory. It appears that there is more
agreement on the role of sleep in reinforcing procedural memories (the acquisition of
skills, tasks, and expertise) and less with declarative memory (facts, knowledge, and
episodic details of an event) (Stickgold et al., 2000).
Walker (2005) provides a theoretical framework with which to understand much of this
inconsistency by differentiating between three stages of memory: an acquisition process
that occurs mainly (and most effectively) in wake but can be shown during sleep, a
stabilization process that takes place following acquisition and is reliant on the passage
of time rather than sleep, and an enhancement process that is dependent on sleep.
Following acquisition of a procedural skill, a memory trace is believed to be fragile,
requiring further reinforcement. This reinforcement is understood to take place over a
period of between 15 minutes to 6 hours following skill acquisition. Between skill
acquisition and stabilization that memory is vulnerable, and further consolidation is not
guaranteed. An example of how this works is offered by Muelbacher et al. (2002) in
which, following acquisition of a motor skills task, participants showed expected
improvement in task performance at the end of a training session. This was persistent on
retest after a 15-minute interval. However, interference for one group using repetitive
transcranial magnetic stimulation (rTMS) during the 15-minute interval resulted in a
return to pre-training levels of performance. Furthermore, when an additional group of
participants underwent the same interference technique, but this time at 6 hours
following the end of the training session, performance was found to remain at post-
training levels. It is assumed, therefore, that the stabilization process occurs sometime
between 15 minutes and (p. 68) 6 hours, and that certainly by the 6-hour point that
memory is no longer vulnerable to the distraction of an interference process. Prior to
stabilization, the memory can be lost. In no condition did performance actually improve
from post-training levels. Further evidence suggests that memory for visual and motor
procedural skills gained during training can persist throughout up to 12 hours of wake
(Walker et al., 2002, 2003).
Perhaps more remarkably, there is growing evidence to show improvement in

performance without further training, following a night of normal sleep (Karni et al.,
1994; Brashers-Krug et al., 1996; Shadmehr & Brashers-Krug, 1997). To counter criticism
of a time-dependent rather than sleep-dependent mechanism involved in this
improvement, Walker et al. (2002, 2003), again using a motor task, trained participants at
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either 10 a.m. or 10 p.m. As expected, there was an effect of training with a 60%
improvement in performance for both groups at the end of the training session. Both
groups were tested again following an intervening 12-hour period. For the 10 a.m.
morning training group this intervening period was made up entirely of wake.
Performance indicated that stabilization but not enhancement had taken place, with
levels similar to that of the end of the training period. In contrast, participants trained at
10 p.m. showed improvement in performance (20% speed, 39% accuracy) at 12 hours
post-training, following an intervening night of sleep. At 24 hours post-training, the
morning group, having now had the opportunity to sleep, showed similar improvements
to the night-training group at the 12-hour post-training trials. However, the night-training
group showed no further benefit at the 24-hour post-training trials. These authors
conclude that the additional learning (delayed in the morning group despite the
equivalent interval between tests) is facilitated by the opportunity for sleep, and not
simply the passage of time.
Will any sleep state suffice to facilitate enhancement? Walker et al. (2002) found a
correlation between magnitude of improvement and time spent in stage 2 NREM sleep as
a proportion of overall sleep time. But this is not consistent with other studies, and it is
suggested that task complexity and sensory demands are likely to account for these
inconsistencies. Further evidence of performance improvement following sleep covers
visual discrimination tasks (Karni et al., 1994), visual motor skills (Maquet et al., 2003),
and auditory tasks (Atienza et al., 2002, 2003).
There are some difficulties with the design of the Walker (2002) study, in particular with
the introduction of time of day of training and testing as a potential confound (Siegel,
2005). Coenen (2005) also argues that the Walker (2002) study does not provide evidence
of an active role for sleep in the enhancement of memory, but that the effectiveness of
sleep may be in providing a period of time free from the competing distraction of
interference. In that sense, sleep is considered to be a passive process, favorable, but not
essential, to the enhancement of memory.
Having to some extent predicted this argument, Walker (2002, 2003) studied a third
group of participants who were this time requested to wear mittens between 10 a.m.
training and 12-hour post-training trials. This simple measure was intended to inhibit the
use of motor skills between trials, as might happen if the main role of sleep was to
eliminate or greatly reduce the demand on related motor circuitry. If, in this scenario,
sleep simply dampens motor activity to allow enhancement, one might expect the mittens
to be an effective alternative in achieving this end, even during wake. This was not found
to be the case, as the absence of hand movements during wake did not lead to further
enhancement of performance. However, following a night of sleep, this group showed
improvement at the 24-hour post-training trial.
Critics of this view of sleep-dependent memory processes point to the many studies that
have failed to establish this link between an essential need for sleep prior to
enhancement, including Atienza et al. (2005), in which performance on an auditory
Page 13 of 26

discrimination task was enhanced despite 48 hours of sleep deprivation, and Doyen et al.
(2005), who found that the passage of time was sufficient for improvement on a motor
task. It has also been argued that while REM deprivation or suppression does not lead to
memory impairment, nor do learning challenges increase the need for REM sleep. We
might think back to the argument put forward by Kavanau (2005) in which he advocates
that NREM memory processes, while more primitive and inefficient, take over in the
absence of REM. Does this explain inconsistencies in attributing enhancement processes
to sleep states (Walker, 2005), and is there sufficient evidence to show an essential role
for sleep in memory function?
Piggott and Perry (2005) point out further obvious inconsistencies with the sleep-
dependent memory process position, this time from the clinical field and including studies
that show that insomnia is (p. 69) not consistently linked with poor memory, that
pharmacologically increased total sleep time does not lead to improved memory, that the
sleep disturbances of Parkinson’s disease are not related to memory dysfunction, and that
normal age-related reduction in total sleep times is not correlated with memory deficit.
Vertes (2005) is also critical of sleep-dependent memory process on the strength of

current evidence arguing instead that “at best consolidation based enhancement [of
memory] is a slow, time-dependent process of consolidation that begins with task
acquisition in waking and can under some circumstances extend to sleep” (p. 86). We are
again reminded that REM sleep does not increase following a heavy learning challenge,
and that memory problems do not follow from the artificial suppression of REM sleep.
While we assume that an intervening night of sleep is responsible for improvements in
procedural skills in an experimental setting, improvements without further practice will
occur over time anyway, suggesting that some aspect of consolidation is achievable
during wake. Interference and distraction are important issues in the formation of
memory, but there is insufficient evidence at this time to assume that the role of sleep is
anything other than to minimize their effect and that, given favorable conditions, this
could be achieved equally well during restful wake (Vertes, 2005; Vertes & Siegel, 2005).
Is all sleep essential?
Before moving on, it is perhaps important to point out that not all sleep researchers are
currently absorbed by this debate and that, for some, the role of sleep and memory is
largely overstated. Somewhat reminiscent of his earlier work on core and optional sleep,
Horne (2006) has recently advised that “… our sleep alters as a night’s sleep progresses,
initially serving important purposes, changing to those of less benefit, and eventually to a
sleep that is superfluous, luxurious and just pleasant to take” (p. 893). We can assume
from this that as the latter stages of sleep comprise mainly REM and stages 1 and 2
NREM sleep, at least some part of a nightly NREM and REM quota is understood to have
little essential function.
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The role of the NREM rebound following sleep loss is believed to be compelling evidence
in support of a restorative role for sleep (Borbely & Tonini, 1998). The need for sleep is a
function of both homeostatic and circadian processes, increasing throughout the day
largely independent of cognitive or physical activity. Time awake is the critical factor in
terms of the NREM rebound, i.e., increased duration and intensity of NREM periods,
usually in the first half of the night, in response to increased periods of wake. Increased
intensity of slow-wave activity is predominant in the frontal regions of the brain and has
been linked with deterioration in executive-type skills following sleep loss (Muzur et al.,
2002). The reverse, reduced duration and intensity of delta activity in the first two cycles
of sleep, has also been shown following reduced periods of wake time between sleep
episodes (Harrison & Horne, 1996). However, contrary to expectations, and as has been
described earlier, the NREM rebound is not universal across species. For rats and
pigeons, a REM rebound is observed following sleep loss, whereas migratory birds or
those experimentally deprived of sleep show no sign of rebound sleep (Siegel, 2008).
Short and long sleepers have comparable amounts of slow-wave sleep. Differences in
sleep architecture lie in the amounts of REM and stages 1 and 2 NREM sleep (Borbely &
Tonini, 1998), suggesting that they are better able to tolerate longer wake periods with
few difficulties in terms of physiological or cognitive performance, while satisfying an
essential need for sleep within a shorter sleep episode. Interestingly, there was some
controversy, first voiced in the 1970s (Webb & Agnew, 1975; Carskadon & Dement, 1979),
gathering momentum in the 1980s (Carskadon et al., 1986; Roehrs et al., 1989) peaking
in the mid-1990s (Bonnet & Arand, 1995; Harrison & Horne, 1995; Roehrs et al, 1994),
and continuing more recently (Balkin et al., 2008; Banks & Dinges, 2007; Klerman & Dijk,
2005; Van Dongen et al., 2003; Vgontzas et al., 2004), concerning the question of whether
the general population of the Western world was getting enough sleep. The view that
many individuals are chronically sleep deprived rested on the assumption that as humans
could be encouraged to sleep more than their habitual amount, this extra sleep was
probably necessary, with sole benefits in terms of relief from subsequent objectively
defined sleepiness (although mainly during the combined influence of circadian “low
points”). This debate is likely to continue for some time as researchers continue to
question the relationship between sleep and daytime waking function.
In terms of more acute, total sleep loss, much research has focused on the specifics of
cognitive deficits, whether it be to memory systems, attention, arousal, or more
generalized performance. In recent (p. 70) years, brain imaging studies highlighted the
importance of changes to specific regions of the brain during sleep or periods of sleep
loss (Maquet, 2000; Thomas et al., 2000; Drummond et al., 2000, 2001, 2004), and this
knowledge has guided the direction of neurocognitive studies investigating behavioral
correlates of these changes. To some extent, this approach has also been useful in
understanding individual variability in performance deficit following sleep loss (Chuah et
al., 2006).
Page 15 of 26

It has been shown that sleep loss in humans leads to performance decrements across a
range of cognitive processes including memory (Chee et al., 2006; Durmer & Dinges,
2005; Harrison & Horne, 2000a, b Lieberman et al., 2006), psychomotor vigilance and
attention (Casagrande et al., 2006; Dinges, 1991; Lim & Dinges, 2008; McCarthy &
Williams, 1997), executive function, (Espelid & Harrison, 2001; Harrison & Horne, 1997,
1998; Jones & Harrison, 2001; Killgore & McBride, 2006; Wimmer et al., 1992), and
group and individual decision making (Baranski et al., 2007; Barnes et al., 2009; Harrison
& Horne, 1999, 2000a, b). Mood and related subjective experience, such as frustration,
emotional judgment, and poor interpersonal skills (Huck et al., 2006; Kahn-Greene et al.,
2006) are also reported to deteriorate with sleep loss (Pilcher & Huffcutt, 1996; Franzen
et al., 2008). Although some effects appear to be reduced by caffeine and other stimulants
(Caldwell & Caldwell, 2005; Harrison & Horne, 2000a, b Huck et al., 2008; Kamimori et
al., 2005; McLellan et al., 2005; Wesensten et al., 2005; Wyatt et al., 2004), the
involvement of non-sleep-related factors such as arousal, motivation, and stress are rarely
considered to be serious enough to undermine the validity of this approach.
We know from earlier studies of rats (Rechtschaffen & Bergmann, 1995) that death will
eventually follow from long-term total sleep deprivation, but the mechanisms leading to
death have never been clearly elucidated. The assumption that death would be the end
point for all species undergoing total sleep deprivation is generally accepted, though
rarely put to the test. However, Rial et al. (2007) questioned the basis of this assumption
by pointing out that the protocols of many animal-based sleep-deprivation experiments
mirror conditions conducive of a learned helplessness, in which acceptance of
unavoidable punishments result in stress-related physical decline and eventual death. In a
learned helplessness paradigm (originally proposed as a model for the development of
depression [Seligman, 1968]), the individual animal is typically unable to escape from
negative outcomes, such as an unavoidable electrical shock. Compared with control
animals that learn to move toward areas of safety, the experimental animal will eventually
succumb to the inevitability of the situation and lose their will to search for an answer to
their predicament.
Given that the strategies for keeping animals awake are likely to be both stressful and
run counter to a very strong drive to sleep, or at least remain inactive, it seems
reasonable to question the contribution of non-sleep-related factors, such as fear, stress,
and loss of interest, to eventual outcomes. Of course, there is a huge difference in
comparing rodent with human sleep loss studies in terms of informed consent and the
ability to withdraw from involvement at any time, should they so wish. Nevertheless,
withdrawal from human sleep loss studies, reportedly unusual, is always at some cost,
whether in the form of tangible rewards such as financial gain or university course credit,
or disappointment at being unable to fulfill a commitment to experimenters or oneself to
complete the task. The pressure to remain within an experiment and the subsequent
effects on motivation and compliance are rarely considered, whether in terms of mood or
performance. As a consequence, the idea that all sleep provides some vital function is
Page 16 of 26

widely accepted on the basis of studies that show deleterious effects in humans and
animals, whether acute, total sleep loss, or what is considered to be chronically restricted
sleep.
Rial et al. (2007) argues that the fatal consequences of sleep loss in rats, assumed to be
an indication of the physiological necessity of sleep, are in fact a manifestation of learned
helplessness in these animals, and that we are misguided in generalizing these findings to
other species, particularly humans. They suggest instead that the functions of sleep are
overstated and may in fact be more “trivial” than might be expected.
In their view, animal death during sleep loss is likely to be stress related, and similarly,
cognitive impairment in humans (e.g., memory, attention, vigilance, mood) can also be
accounted for largely in terms of the artificially induced stresses of the experimental
paradigm and are not specific or unique to sleep function. They go on to propose that rest
is sufficient for many animals and, particularly in cold-blooded animals, is largely dictated
by environmental necessity rather than a homeostatic function of sleep. They further
suggest that we have no direct evidence from sleep loss studies of the (p. 71) necessity
of sleep, which they describe as “… a junkyard in the evolution towards cortical
conscience” (p. 322).
Conclusions
Clearly there is still no consensus on the functions of sleep in humans or other animals,
with ideas ranging from sleep as a vital process, necessary primarily for the maintenance
and enhancement of memory function, to the view that sleep has some adaptive
advantage, which is likely to be different between animal types and within specific
environments. For humans, the argument in terms of cerebral restitution is intuitively
attractive, but there are difficulties with the assumption that sleep loss, even in a
cooperative participant (who already has some idea of likely effects), will reveal deficits
unique to that state. Many studies have shown the effects of sleep loss to be small and
difficult to replicate, with well-known psychological effects (e.g., end of trial, placebo,
practice, stress, etc.) often ignored. Enthusiasm for the relationship between sleep and
memory process is ongoing and appears to fit with a more ecological view of why we
sleep, and yet again the inconsistencies and lack of replication studies are a problem for
this approach. There is a commonly held assumption that many people would like, and
will perhaps benefit from, more sleep, yet subjective experience can be misleading as, in
the public view, this is often difficult to separate from the more general stresses of daily
life.
We see something of this capacity to modify sleep duration in adult humans, who are able
to tolerate change that is predictable, regular, and non-stressful (e.g., as with extended
sleep studies such as Wehr et al., 1993; Roehrs et al., 1989, 1994). Similarly, around the
1970s a number of studies showed that when change was introduced gradually, it was
Page 17 of 26

possible to achieve a reduction in habitual sleep length of approximately 2–2.5 hours with
little ill effect (Webb & Agnew, 1965; Friedmann et al., 1977; Johnson, 1973; Johnson &
MacLeod, 1973; Mullaney et al., 1977). So within limits, humans also appear to be flexible
in their sleep need, suggesting some support for the view that at least part of a nightly
sleep is dispensable, under the right conditions. The experience of reduced or total sleep
loss will depend to a great extent on related stressors (such as following childbirth or
throughout consolidated exam periods). We also see change in sleep need with age. The
high proportion of infant REM sleep, correlated with immaturity at birth in primates
(Siegel, 1995), shows a rapid decline in the first 6 months of life, suggesting that sleep
may serve a number of functions across the life span.
We are left with the difficulty of explaining the ability of some animals to manage
perfectly well without sleep, under certain conditions, and usually dictated by feeding or
reproductive strategies. Clearly the question of whether sleep is a physiological necessity
is relative to other factors, some of which are environmental. The issue is also clouded by
the suggestion that functions believed to be dependent on sleep might also be effectively
performed during a period of restful wake. Developments in this area will rely on greater
clarity over what functions (physiological or cognitive) are achieved only with the benefit
of sleep, and those that might benefit from aspects of sleep but are not entirely
dependent on this state.
Future directions
1. Inconsistency in experimental findings of memory, vigilance, and other cognitive
functions might be addressed by taking greater account of the role of stress and
motivation in controlled sleep loss studies.
2. With the above in mind, researchers should endeavor to design experimental
studies that allow the separation of those aspects of memory function that are
achievable during wake and those that are essentially sleep dependent.
3. To allow further comparisons both between and within species, noninvasive
studies of animal sleep behaviors should take place as far as possible in their natural
environment and be expanded to take into account factors likely to impact on sleep
variability such as changes in season, climate, food availability, and mating
strategies.
Related chapters
Chapter 1 (Sleep and the Brain)
Chapter 2 (The Regulation of Human Sleep and Wakefulness)
Page 18 of 26

Chapter 5 (Sleep and Human Performance)
Chapter 6 (The Role of Sleep in Neurocognitive Function)
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Sleep and Human Performance

Timothy H. Monk

This chapter discusses different ways in which human sleep and performance are
interrelated. First there is a discussion of the role of sleepiness and performance
decrements at the end of the waking day as messengers and sanctions by which a regular
circadian patterning of sleep and wakefulness is encouraged. Next there is a discussion of
performance decrements soon after awakening from sleep (sleep inertia), and the “post-
lunch dip” in performance that can sometimes arise when the early afternoon (siesta)
gate to sleep is open. There then follows a discussion of the effects on sleepiness and
performance of total sleep deprivation (TSD), when one or more whole nights of sleep are
missed, and chronic partial sleep deprivation (CPSD), when sleep is abbreviated for a
week or more at a time. The chapter ends with a discussion of the practical real-life
consequences of fatigue-related performance failures, particularly in transportation and
medical care.
Keywords: sleep, sleep deprivation, performance, alertness, sleepiness, circadian
Sleep and performance as an issue

Sleep is like oxygen. When we get about the right amount of it, we do not think about it
much; but when we get too little (or even too much) of it, then problems occur, often
including a failure to perform properly. We do not think about getting enough oxygen
when we are getting enough oxygen. It is the same way with sleep. Usually, we pay
attention to how sleep and performance are related only when we are not getting the
right amount of sleep. In the case of oxygen loss, what gets our attention is the onset of
panting and lightheadedness; in the case of sleep loss, it is the mechanism of subjective
sleepiness that gets our attention. Thus, the focus of this chapter is on not only what
Page 1 of 24
Subscriber: Freie Universitaet Berlin; date: 01 November 2018

happens to human performance when we are not getting enough sleep, but also what
happens to subjective sleepiness, since that is the messenger, as it were, by which we are
made aware of our sleep insufficiency. Just like panting increases our uptake of oxygen,
though, the eventual aim of subjective sleepiness is also the rectification of the sleep
insufficiency, i.e., the promotion of sleep per se. This can be very dangerous if we are, for
example, driving a car, but can be beneficial if it spurs us to go to bed at the correct
circadian time.
One can make a distinction between sleepiness and fatigue, although the two terms are
often used interchangeably. Perhaps the main feature of fatigue, distinct from sleepiness,
is that although fatigue may lead the individual to desire sleep, fatigue is often not
dissipated by that sleep. Thus, fatigue usually has disease-based (e.g., chronic fatigue
syndrome, depression) or substance-based (e.g., antihistamines, alcohol) etiologies that
are not dependent on the preceding amount of sleep actually obtained. As thus defined,
fatigue will not be discussed in this chapter. Instead, we shall use the terms sleepiness
(and its converse alertness), implicitly assuming that such constructs specifically concern
everyday life influences of sleep and circadian rhythms, rather than influences of
pharmacology or disease.
The above discussion does, of course, represent an oversimplification. Sleepiness does

not occur only when insufficient sleep is being obtained. It also (p. 96) occurs at either
end of the nocturnal sleep episode and during the early afternoon “post-lunch dip.” At the
front end of the nocturnal sleep episode, in a willful and inquisitive species such as H.
sapiens, the sanction of sleepiness can be regarded as a necessary tool for imposing the
correct circadian patterning of sleep–wake behavior (see Chapter 2). Without it, we would
simply be like the playful puppy that goes on running until sleep overtakes it and causes
it to drop in its tracks. For human society to function well, that irregularity in sleep–wake
patterning cannot be tolerated. Indeed, for untreated narcolepsy patients whose disease
often does, quite literally, cause them to drop in their tracks (see Chapter 31), our world
is not an easy place in which to live.
Performance and alertness changes as

harbingers of sleep
In his 1941 classic short story “Nightfall,” Isaac Asimov describes a planet with six suns
that cause it to normally be in a state of continuous daylight. Every two thousand years or
so, there is an eclipse, and darkness briefly occurs across the planet with disastrous
consequences for society. A main theme of Asimov’s story is about how the inhabitants
reacted to suddenly seeing stars and realizing that they are not alone and that there is a
whole universe out there. To a circadian rhythms researcher, the more telling question,
though, is that of how the inhabitants of that imaginary planet would structure time
throughout their lives. How would they create milestones in their lives without nights and
Page 2 of 24

days? If they evolved on such a planet, would there be anything akin to circadian
rhythms? Or would they simply behave like the playful young puppy mentioned above,
and simply run until they drop? Our evolution on a planet with a 24-hour alternation of
daylight and darkness has had a profound impact upon not only our physiology and
behavior, but also how we think about time.
Different species exhibit different sleep–wake patterns, so that they have a temporal
niche that is “theirs” and so that they are up and about when prey can be caught (see
Chapter 2). Unsurprisingly for such a visually dominated species, the temporal niche for
H. sapiens is the daylight hours (Moore, 1997). We are a diurnal species, designed to be
asleep during the darkness of night and awake during the daylight hours (perhaps with a
nap after lunch—see below). This has allowed us to consolidate sleep into a ∼7-hour span
during the night hours. As we have learned from recent work (see Chapter 6), this has
had important positive effects regarding our ability to learn. What it also means, though,
is that throughout our evolutionary development as a species, it has been necessary for
us to find ourselves, each evening, somewhere safe to sleep at night so that we don’t get
attacked by predators, get soaked with rain, or freeze to death. Importantly, this behavior
needs to anticipate nightfall. If we wait until it is dark and/or we are about to drop in our
tracks from exhaustion, we have waited too long. Thus, we have a circadian system that is
exquisitely tuned to start shutting things down prior to the sleep episode, and to inform
us that we need to start bed-seeking behavior well before we actually fall asleep. The
messenger for that signal is an increase in subjective sleepiness (or decrease in alertness)
and a degradation in our ability to perform. One remembers the old drinking song: “Show
me the way to go home [cognitive failure], I’m tired [subjective sleepiness] and I want to
go to bed [bed-seeking behavior].” Thus, one important link between performance
(including subjective sleepiness/alertness) and sleep is that of a circadian signaling
mechanism, allowing a communication between the circadian system and the conscious
mind. Thus, the circadian system makes its wishes known to the conscious mind via
changes in alertness and performance. The essence of circadian rhythm sleep disorders
(see Chapters 28 and 29) is that there is a breakdown in this signaling mechanism, such
that the individual is not ready for bed at the time when he or she needs to be (delayed
sleep phase syndrome—DSPS), is ready for sleep earlier than he or she wants to be
(advanced sleep phase syndrome—ASPS), is working a schedule that violates his or her
diurnal nature (shift work sleep disorder), or has rapidly crossed several time zones (jet
lag sleep disorder). Because of the pivotal role of performance and subjective sleepiness
changes in the patterning of sleep and wakefulness, each of these four circadian rhythm
sleep disorders necessarily leads to increased sleepiness and performance decrements at
times when they are unwanted by the individual.
Page 3 of 24

As noted above, the level

of an individual’s
sleepiness/alertness varies
as a function of time or
day. Importantly, though,
this is not simply a “step
function” whereby
alertness levels are
relatively constant through
the daylight hours and
abruptly decline a few
Click to view larger
hours before bedtime.
Fig. 5.1 Time of day effect in subjective alertness (n
= 98) after Monk et al. (1994). When measured only over
the normal waking day,
alertness shows a gradual rise from bedtime to midday, with a subsequent decline that
ends in the lowest level, just prior to bedtime (Figure 5.1). If one samples alertness
beyond bedtime, the circadian alertness rhythm continues (p. 97) to decline, reaching a
trough at about 4–6 a.m., with a subsequent rise thereafter (upon which, of course, is
superimposed an overall declining trend from being awake all night) (Monk et al., 1997).
That morning rise is colloquially referred to as a “second wind.” In fact, of course, it is
simply the circadian clock revving up the system for an anticipated wake time, even
though the individual is yet to fall asleep. As we discuss later (see Figure 5.7), this
function is (not coincidentally) predictive of the circadian rhythm in single-vehicle motor
accidents (Mitler et al., 1988). Thus, as we noted at the beginning of this chapter, if we
ignore our bedtime and remain up and about, the circadian system sends ever more
forceful messages that we should be asleep.
One problem in assessing alertness and performance is that people do not perform, and
cannot report how alert they are, while they are actually asleep. However, if individuals
are deprived of sleep, they show alertness and performance decrements during the night
hours, some of which can be attributed to progressively increasing sleep loss, rather than
to circadian effects per se. One way around this is to allow subjects to have brief 30-
minunte naps, interspersed with 60 minutes of wakefulness around the clock (i.e., a 90-
minute rather than a 24-hour “day”). This technique allows circadian alertness and
performance rhythms to be sampled in wakefulness during each of the 60-minute “day
times.” From this sampling one can glean 24-hour rhythms in alertness and performance
without the contaminant of sleep loss. As shown in Figure 5.2 (adapted from Buysse et al.,
2005), there is a circadian rhythm in subjective sleepiness that is a continuous curve,
rather than simply an abrupt step function. Importantly, circadian rhythms in subjective
sleepiness and objective performance are of non-trivial magnitude.
Page 4 of 24

Sleep inertia
As well as heralding sleep
by declines as the
individual approaches
bedtime, there are also
transition effects with
regard to alertness and
performance as the
individual emerges from
sleep and has to perform.
Few individuals can wake
up and immediately
function at 100%. Usually
Fig. 5.2 The circadian rhythm in subjective
sleepiness in individuals living on a 90 min “day”,
there is first a brief period
with 60min awake and 30min asleep (after Buysse et of grogginess referred to
al., 2005).
as “sleep inertia.” Because
of their operational
significance, sleep inertia effects on performance have long been a topic of empirical
study (e.g., Wilkinson & Stretton, 1971). The recovery function from sleep inertia can be
represented by (p. 98) a saturating exponential function with an asymptote at about 2
hours after awakening. For all intents and purposes, though, sleep inertia effects
(although still detectable) are usually fairly negligible after about one hour (Jewett et al.,
1999). In Jewett et al. (1999), the time constant was found to be 0.67 hour for subjective
measures, and 1.17 for objective performance. These figures are in line with the time
constant value of 0.66 used by Folkard and Akerstedt (1992), whose mathematical model
of alertness included (in addition to circadian [C] and homeostatic [S] processes) a
process W from sleep inertia modeled by a saturating exponential function. Recently,
Wertz et al. (2006) showed that up to 20 minutes after wakening the sleep inertia effect
(in a cognitive task) was equivalent in magnitude to the effect of staying awake an entire
night. From 21–61 minutes, however, performance was 83%–86% of peak value and was
not significantly different from the other time points. Thus, although quite important very
soon (<30 min) after awakening, in most cases sleep inertia effects can be regarded as
fairly minimal thereafter. However, the size and duration of the sleep inertia effect does
depend upon the age of the subject, the circadian phase at which the awakening takes
place, and the sleep stage from which the individual is awakened—all of which can
increase the magnitude and duration of the sleep inertia effect (Silva & Duffy, 2008).
Performance dips at “siesta” time
Page 5 of 24

Although much of the forgoing discussion has been concerned with sleep at night, it is
also worth noting that many (if not most) of the human beings on this planet regard the
early afternoon as a suitable time for a short sleep. There is some tendency toward
latitudinal chauvinism, particularly in North American and Northern European cultures,
regarding monophasic sleep patterns as being the norm for all human beings. This view
conveniently forgets that as a species, H. sapiens first evolved in very hot areas of the
world, where it makes a lot of adaptive sense to have a nap during the early afternoon
heat of the day. In Northern cultures this afternoon nap tendency is labeled the “post-
lunch dip” and is often regarded as being somewhat degenerate. However, as argued by
Dinges and Broughton in their influential treatise on napping, even without alcohol at
lunchtime (or even any lunch at all), there is an increased propensity to sleep during the
early afternoon hours that appears to be general to human beings, whatever their home
latitude (Dinges & Broughton, 1989).
A number of different strands of empirical evidence weave together to build a case for an
afternoon nap propensity to be universal. In Campbell and Zulley’s disentrainment
studies (Campbell, 1984), subjects in a totally unstructured temporal routine still chose to
sleep more in the post-lunch dip (even though there was no lunch). Lavie (1991) has
demonstrated a secondary “gate to sleep” in the early afternoon in ultra-short (7 minutes
asleep, 13 minutes awake) sleep–wake cycle studies. Increased sleep propensity in the
early afternoon is also evidenced by the classic “M-shaped” time of day function observed
in the Multiple Sleep Latency Test (MSLT) at which sleep onset latency is measured at
intervals over the day. The early afternoon test time is almost universally associated with
relatively short sleep latencies, suggesting a higher level of sleep propensity during the
early afternoon (Richardson et al., 1982). Moreover, Carskadon and Dement (1992) have
shown that the post-lunch dip still occurs, even when the subject is on a constant routine
with no knowledge of time of day and no “lunch.” Thus, even if the individual comes from
a temperate non-siesta culture and has not had a heavy lunch, there will be an extent to
which he or she is fighting off the desire for sleep. Not surprisingly, this may serve to
impair his or her performance and/or alertness.
From laboratory studies there is some empirical evidence for a post-lunch dip in
performance, although its presence appears to be less universal than in measures related
to sleep propensity. Blake’s classic 1960s studies (Blake, 1967) of performance and time
of day showed a clear post-lunch dip in measures of card sorting, serial search, and signal
detection. Colquhoun (1971) also showed the effect to be present, even in the absence of
a meal. The phenomenon was further studied by Craig (1981) who demonstrated, in a size
judgment task, that the effect could be worsened by taking a high-carbohydrate lunch,
but that the effect was still present, even with a light lunch. Post-lunch dip performance
effects were also studied by Christie and McBrearty (1979) who were, however, not able
to find a clear post-lunch effect, finding instead rather complicated gender- and
personality-related correlations. In a similar vein, when Folkard and Monk (1985)
performed a meta-analysis of time of day effects in various laboratory measures of
performance efficiency, there was little evidence of a clear post-lunch dip. Moving to
“real-life” field data, the evidence for a post-lunch dip becomes more compelling. Both a
Page 6 of 24

collection of actual-task circadian performance curves (Folkard & Monk, 1979) and an
international (p. 99) meta-analysis of traffic accidents (Mitler et al., 1988) show evidence
for a post-lunch dip in performance. Here, however, the post-lunch dip in performance
might have been more related to unintended bouts of sleep rather than a general slowing
of responses. Indeed, it is the boring, monotonous (i.e., sleepiness-inducing) tasks that
are the ones most likely to show a post-lunch dip in performance.
In conclusion, it would seem that performance decrements occurring at siesta time in

non-napping subjects do occur but are not universal, despite there being strong evidence
for universal sleep propensity effects. In our 1996 study of post-lunch dip performance
effects (Monk et al., 1996), we found that some healthy young adult subjects showed a
post-lunch dip in performance at a monotonous vigilance task (“dippers”), while others
did not (“non-dippers”). Our subjects were continuously awake, semi-recumbent, and time
isolated, with meals replaced by hourly nutrition drinks. Under these conditions, it
appeared that it was the strength of the 12-hour harmonic components of the circadian
temperature rhythm that determined whether or not the individual was a “dipper” in
terms of performance. This reinforces the endogenous nature of the post-lunch dip, as
well as the importance of considering circadian rhythm effects when discussing the link
between performance and sleep.
Performance after total sleep deprivation

(TSD)
As discussed by Dinges and Kribbs in their review of sleep deprivation effects on
performance (Dinges & Kribbs, 1991), there are several challenges that affect one’s
ability to accurately determine the effects of total sleep loss on performance. The first
relates to circadian rhythms. As we have noted earlier, there are circadian rhythms in
performance that comprise gradual changes over the entire 24 hours and that are of non-
trivial magnitude. Thus, one must be careful to compare rested and sleep-deprived
conditions at the same time of day. As we have seen earlier in the chapter (e.g., Figure
5.2), alertness and performance during the night hours may be impaired, even when
subjects are not kept continuously awake (Buysse et al., 2005). The second problem
relates to “practice effects” or “learning curve effects.” If the sleep-deprived performance
assessment always follows the well-rested assessment, then the sleep deprivation effect is
likely to be underestimated because practice effects will be improving performance
during that (second) assessment. The third challenge relates to subjects’ abilities to “grit
their teeth” and manage to perform acceptably for the brief period of time needed for the
performance test, after which they “crash.” Because of this, Wilkinson (1966) concluded
that TSD performance effects were more likely to be evident in prolonged tasks lasting 30
minutes or more.
Page 7 of 24

Partly because of the above issues, several studies have failed to find TSD effects on
performance and have erroneously concluded that the TSD effect is, at best, very weak.
The error of such a view is nicely illustrated by the meta-analysis of sleep deprivation
effects conducted by Pilcher and Huffcut (1996). Across all types of tasks and dependent
variables, the overall effect size of TSD was a fairly massive 1.37 (n = 143) [an effect size
of 0.8 is considered large]. When considering studies with task durations ≥10 minutes,
the effect size rose to 1.90. The meta-analysis revealed mood to be the most affected by
TSD, followed by cognitive performance and then motor performance.
As illustrated in Figure
5.3, there are four
different pathways by
which TSD can impair
performance. The first,
and most obvious, pathway
is that the subject briefly
falls asleep. As we have
Click to view larger noted earlier, the function
Fig. 5.3 A conceptual model of the various possible
of sleepiness is to promote
pathways in the link between Total Sleep Deprivation sleep, and occasionally
(TSD) and performance impairment.
sleepiness wins that battle
and the individual has a
very brief period of sleep (sometimes referred to as a microsleep) perhaps lasting only a
couple of seconds, when he or she is essentially “off line” and not performing. We shall
refer to this as the lapse pathway. The second pathway relates to a lack of creativity in the
way in which the task is approached. This may lead to the adoption of familiar or “rote”
information processing strategies that no longer adapt to situations that may have
changed, and may thus be suboptimal. Sleep-deprived persons seldom “think outside the
box.” It may also be evidenced by “tunnel vision,” in which attention is overly focused on
one particular aspect of the situation. We shall refer to this as the cognitive rigidity
pathway. The third pathway is through a general slowing in the actual speed in which
information is processed. Even when paying appropriate attention and remaining awake,
subjects may respond more slowly under TSD because their brain has, as it were, slowed
down, or because they are excessively concentrating on accuracy to the detriment of
speed. We shall refer to this as the cognitive slowing pathway. Fourth, there is the losing
motivation pathway. A person will perform only up to the level that he or she wants to at
that particular moment. From both anecdotal reports and empirical observation, we know
that in extreme circumstances, such as (p. 100) warfare or natural disaster, people can
still perform very well even with quite severe TSD. In non-extreme conditions, though,
they may just stop trying. Motivation loss is unique, as a pathway, in that it can both have
direct effects on performance and can also mediate the lapses and cognitive rigidity
pathways. These latter pathways can either be direct effects of the TSD or result from
changes in motivation consequent upon the TSD. It is our view that all four of these
pathways—lapses, cognitive rigidity, cognitive slowing, and motivation loss—are all valid
Page 8 of 24

pathways by which performance can be impaired by TSD. Which one predominates will
depend upon what is being performed, by whom, under what circumstances, and what
the outcome measure happens to be. We shall consider the four in turn.
As Dinges and Kribbs note in their comprehensive review of laboratory studies of TSD
(Dinges & Kribbs, 1991), the lapse pathway has historically been the dominant
explanation for TSD-related performance decrements, dating back more than a century to
the 1896 work of Patrick and Gilbert. Parenthetically, those early authors also observed
effects we would now refer to as cognitive slowing, attention problems, and circadian
performance rhythms. Much research into TSD was conducted during the 1930s and
1940s, with lapses variously described as “blocks,” “pauses,” “delays,” or “gaps” (Dinges
& Kribbs, 1991), but all referring to the phenomenon of brief pauses of non-responding.
More recently, the term “microsleep” has been coined to describe the phenomenon either
as a formal EEG-based definition of very brief sleep lasting up to 30 seconds, or more
loosely as lapses in which the individual is briefly “frozen” or “mentally absent” (Rosekind
et al., 1994). The lapse hypothesis was most clearly articulated by Williams, Lubin, and
Goodinow (1959) in their classic 1950s study of 72+ hours of sleep loss.
Since that time there have been numerous studies of TSD, many finding an increase in
the number of lapses (and thus increase in the variance of response latencies) with TSD.
These lapses may not always be associated with actual sleep, but may instead reflect
wandering attention. In the 1980s, Dinges and colleagues (Dinges & Powell, 1985)
developed a simple serial reaction time task called the Psychomotor Vigilance Task (PVT),
which has shown itself to be particularly well-suited for detecting lapses in performance
and to have the benefit of showing minimal learning curve, or practice, effects (Dinges et
al., 1997). Indeed, in the past two decades, the PVT has become the “gold standard” for
performance assessment, particularly in relation to sleep loss (Belenky et al., 2003; Van
Dongen et al., 2003; Wright et al., 2002). The subject is presented with a display signal
that presents the response latency as it builds up. When the signal comes on the subject
must press a button as quickly as possible; the latency in milliseconds is then displayed,
and after a random interval (2 sec.–10 sec.) the display comes on again and a new trial
starts. Typically, the task is performed for 10 minutes; the main dependent variable is the
total number of lapses, usually defined as response latencies >500msec, although speed
of responding (the inverse of response latency) may also be used.
The second pathway by which performance can be impaired during TSD is that of
cognitive rigidity. (p. 101) Anecdotally, many of us can remember doing something when
sleep deprived that may have been okay normally, but that failed to reflect changed
circumstances and thus became inappropriate. As noted above, it is very difficult to
“think outside the box” when sleep deprived. Empirically, this has been investigated by
Horne and colleagues (Harrison & Horne, 2000; Horne, 1988), who required sleep-
deprived subjects to do tasks that tapped into their ability to think creatively. Among
other variables, Horne (1988) used the Torrance test of creative thinking and compared
performance under well-rested and TSD conditions (always tested the following evening).
Performance was impaired by sleep deprivation: effect sizes for TSD were 1.8 for figural
Page 9 of 24

flexibility and 3.5 for verbal flexibility, with similar robust effects appearing for other
scales of the Torrance and for other measures such as word fluency (effect size 1.8), and
nonverbal planning (effect size 3.3). Further developing the concept of cognitive rigidity
as a pathway to TSD-related performance decrements, Harrison and Horne (1999)
developed a highly motivating marketing strategy game that they gave to graduate
students under both rested and TSD conditions. The TSD condition invariably led to
failure in the game because sleep deprivation led to more rigid thinking, increased
perseverative errors, and marked difficulty in appreciating an updated situation. In their
review of the impact of TSD on decision making, Harrison and Horne concluded that “If,
during a prolonged crisis, key decision makers remain awake beyond about 24 hr, then it
is reasonably clear that despite their best efforts to perform well, their decision-making
ability will become impaired” (p. 247). That conclusion is borne out by a recent meta-
analysis concerning hospital house staff (discussed later in this chapter), where TSD
appears to result in clinical performance decrements in physicians with an effect size of
about 1.5 (Philibert, 2005).
The cognitive slowing pathway by which performance is worsened by TSD is not always
easy to positively identify. Also, it is different from the lapse and cognitive rigidity
pathways in that it is unlikely to be mediated by motivation loss. The essence of this
pathway is the hypothesis that all other things being equal with regard to the task, the
rate of information processing will be slower under TSD. Unless one is careful with the
selection of task given and variable used, cognitive slowing effects may be masked by
effects from the other three pathways. Thus, microsleeps, cognitive rigidity, and
motivation loss may all lead to changes in measured performance that might outweigh
any effects due to the slowing down of information processing rates by the brain. One
way around the problem is to measure the inferred speed of information processing by
measuring performance speed in aspects of the task in which an extra step is required.
This was illustrated in a 1997 study by Monk and Carrier (1997) that involved 18 healthy
young adults experiencing 36 hours of wakeful bed rest, starting at 9 a.m. Every 2 hours,
these subjects completed a test comprising 32 trials of a modified form of the Baddeley
verbal reasoning test—a classic “working memory” task (Baddeley, 1968). The subject had
to press “true” or “false” buttons when presented with sentences purporting to describe a
letter pair (e.g., “M is not before C—CM”). Sixteen of the 32 items were phrased in the
positive voice (e.g., M follows C—MC), 16 in the negative voice (e.g., M does not follow C
—CM). Sentences were randomly shuffled. Irrespective of whether they were true or
false, items phrased in the negative voice took longer to respond to than those in the
positive voice, reflecting the extra processing step that was required of them. Subtraction
of the mean of the 16 positive voice latencies from that of the 16 negative voice latencies
for each subject-test then gave an indication of the calculated extra latency required by
that extra information processing step. Comparisons could then be made of the calculated
speeds during the performance tests given before and after the missed night of sleep, at
each of the “daytime” times of day. Importantly, the derived nature of the speed measure
eliminated effects due to lapses, cognitive rigidity, and motivation loss, which would all
have applied equally to positive-voice and negative-voice sentences within the 32-trial
Page 10 of 24

test. The results are given in Figure 5.4. The calculated speed of cognition appeared to
slow down by between 20% and 60%, depending upon the time of day. In other laboratory
studies of TSD, investigators have also noted that cognitive slowing may sometimes take
the form of a severe slowing in task speed in an attempt to maintain accuracy (Horne,
1988).
As noted in Pilcher and

Huffcut’s meta-analysis
(Pilcher & Huffcutt, 1996),
mood was the variable that
showed by far the largest
effect of TSD in terms of
effect size. Anecdotally, a
loss of motivation and an
Click to view larger excess of negative affect is
Fig. 5.4 The degree of cognitive slowing after one a frequent product of TSD.
night of Total Sleep Deprivation (TSD) at four
different times of day, expressed as a percentage
Rare is the individual who
relative to that time of day (after Monk & Carrier, is not made grumpy by
1997).
sleep deprivation. As noted
earlier, unlike
physiological measures, performance measures are exquisitely sensitive to the goodwill of
the person doing (p. 102) the performing. In extreme emergencies and military
situations, there are powerful incentives to maintain high levels of performance, and in
many such cases performance remains good. However, if the person gives up trying for
any reason, then performance levels will plummet. With very attractive financial
incentives for good performance, Horne and Pettitt (1985) were able to get subjects to
continue to achieve baseline performance levels at a 30-minute auditory vigilance task,
even after 36 hours of TSD. With second and third consecutive nights of sleep loss,
subjects were not able to maintain baseline performance (despite enhanced incentives),
but still performed better than sleep-deprived subjects without incentives. Thus, the
losing motivation pathway is, in many cases, at least a contributing factor to performance
losses after TSD. As shown in Figure 5.3, this contribution may either represent a direct
link between TSD and performance impairment, or act through mediation of the lapse and
cognitive slowing pathways.
Chronic partial sleep deprivation

For most adults who are not night workers, a full night of sleep deprivation is an unusual
event, remembered from the days when one was in college or had small children, but not
a part of current everyday life. Much more common (and becoming increasingly so) is
chronic partial sleep deprivation (CPSD) in which sleep is curtailed for a week or more at
a time. Recent surveys (e.g., Sleep in America Poll, 2000) have revealed the alarming fact
Page 11 of 24

that up to 25% of the population feel that they are not getting enough sleep on a chronic
basis and are experiencing performance deficits and unwanted daytime sleepiness as a
consequence, particularly during the workweek. Often, those experiencing CPSD attempt
to make up for lost sleep on weekends, which may help somewhat with sleep issues but
may be bad for circadian issues. Thus, there is often a “mini jetlag” on Monday mornings
when the workweek schedule of rise times and bedtimes has to be re-established.
Generally, sleep deprivation researchers have tended to concentrate on the “safer bet” of
TSD in order to get significant effects on performance, but there are now several
excellent laboratory studies of CPSD in the literature. Three exemplary studies of CPSD
are discussed below.
Dinges and colleagues

(1997) used the PVT (see
above) to assess
performance in 16 healthy
young subjects whose
sleep was restricted to
67% of baseline levels
Click to view larger (typically to slightly less
Fig. 5.5 Mean sleepiness level and mean PVT lapses than 5 hours) for seven
(see text) during 7 days of Chronic Partial Sleep
consecutive nights.
Deprivation (CPSD) denoted P1 through P7 (after
Dinges et al., 1997). Daytime sleepiness was
also assessed using both
subjective measures and the objective Multiple Sleep Latency Test (MSLT). The restricted
week was preceded by two baseline nights at habitual duration and followed by an ad-lib
recovery night (up to 10 hours). Because the PVT is only minimally affected by practice
(learning curve) effects, the performance assessment was relatively uncontaminated by
such effects. Results for subjective alertness from the Stanford Sleepiness Scale (SSS)
and performance from the PVT (number of lapses) are illustrated in Figure 5.5, which is
reproduced from Dinges et al. (1997). In each case, increases on the Y axis represent
worsened alertness and performance. Thus, as the week of restricted sleep progressed,
performance and alertness progressively worsened in an almost linear fashion. In other
measures, MSLT latencies decreased from an average of 11 minutes on the second
baseline day to 3 minutes on the fifth sleep-restricted day. From the Visual Analogue
Scale (VAS) measures, the greatest effect was observed in the mentally exhausted vs.
sharp dimension. (p. 103) All of the above-mentioned effects were statistically significant.
Dinges and colleagues concluded that CPSD had a dynamic and escalating analogue in
daytime sleepiness and impaired performance, and that a steady state was not reached
within the week of sleep restriction. This is particularly important in that the sleep
restriction (to an average of slightly less than 5 hours) was far from draconian. Clearly
(over 7 nights, at least), young adult subjects cannot “get used to” getting only 5 hours of
sleep. For older adults, of course, our own work has suggested that the limits may be
different (Monk, 2006).
Page 12 of 24

Belenky and colleagues (2003) also assessed alertness performance during a seven-night
CPSD protocol. They used varying levels of sleep duration as modified by changing
allowed Time in Bed (TIB) to 3, 5, 7, or 9 hours TIB for the seven experimental nights
(with about 16 healthy adult subjects per condition). The seven consecutive experimental
nights were preceded, and followed, by 3 nights of 8-hour TIB. Performance was again
assessed by the PVT, and alertness by the SSS and MSLT (amongst other measures).
Results are shown in Figure 5.6, which is reproduced from Belenky et al. (2003). Again,
increases on the Y axis represent a worsening in alertness and performance. As was the
case with the Dinges study, when sleep was restricted (to 7, 5, or 3 hours TIB), there was
an escalating level of sleepiness and performance impairment that was not seen in the 9-
hour TIB condition. Even in the 7-hour condition there was a statistically significant
worsening effect over successive sleep-restricted days. Moreover, the level of escalation
(slope of the increase) showed a dose-response relationship, with the slope progressively
increasing from 7 hours to 5 hours and from 5 hours to 3 hours. Thus, the more that sleep
was restricted, the quicker was the progressive worsening of alertness and performance
over the week.
Van Dongen and colleagues (2003) lengthened the time of sleep restriction from 7 days to
14 days, considering TIB durations of 8 hours, 6 hours, and 4 hours, and comparing CPSD
effects on performance and alertness with that seen in two consecutive nights of TSD.
Again, amongst other measures, performance was measured using PVT lapses, and
alertness using the SSS. Van Dongen et al. showed that for the second week of 4-hour
TIB, the PVT performance decrement was equivalent to that seen after two consecutive
nights of TSD, and that for the second week of 6-hour TIB, the PVT performance
decrement was equivalent to one full night of TSD. Interestingly, though, this effect was
attenuated in subjective measures such as the SSS, which reached an asymptote at the
one night of TSD level. This illustrates the problem of individuals failing to realize how
impaired they are in sleep loss situations, a phenomenon of particular importance when
real-life performance and safety issues with regard to sleep loss are considered. This
study was important in definitively showing that performance indeed suffers in CPSD
situations, and does so in levels equivalent to that seen in TSD situations.
Practical consequences of fatigue-related

performance failures
Falling asleep
Page 13 of 24

As noted at the beginning

of this chapter, subjective
sleepiness is not only a
messenger regarding
insufficient sleep, but is
also a powerful force to
rectify the situation by
putting the individual to
sleep. Perhaps the two
most dramatic examples of
operators being (p. 104)
asleep when they should
have been awake are the
airliner full of passengers
that over-flew its U.S. West
Coast airport and headed
Fig. 5.6 Mean SSS sleepiness score and mean
number of lapses in PVT performance (see text) out over the Pacific with
during 7 consecutive nights with controlled Time In all of the flight crew
Bed (TIB) (see key) (after Beleny et al., 2003).
asleep, and the Peach
Bottom nuclear power
plant in Pennsylvania, where regulators made an unexpected visit one night only to find
everyone in the control room asleep (Lauber & Kayten, 1988). Although fairly hair-
raising, these examples are not, however, the most tragic. The most tragic are the
literally thousands of long-haul truck drivers every year who fall asleep at the wheel, run
off the road, and die. From data reported by Bonnet and Arand (1995), one can glean the
conclusion that fatigue can be directly blamed for the deaths of about 2,700 U.S. truck
drivers per year. As can be seen from Figure 5.7 (taken from Mitler et al., 1988), which
plots the number of fatigue-related vehicle crashes as a function of clock hour, there is a
peak during the very early morning hours that reflects the circadian nadir in alertness
and performance (see Figure. 5.2). Parenthetically, in reference to performance dips
during the siesta interval (see above), Figure 5.7 also reveals a secondary peak in
accidents during the early afternoon hours, which may indicate the effects on driver
performance of an opening of that secondary gate to sleep.
Page 14 of 24

In one of the most

Fig. 5.7 Time of day effect in fatigue-related traffic
accidents from various international sources (after
comprehensive studies
Mitler et al., 1988).
ever undertaken of truck
drivers’ sleep, Mitler et al.
(1997) (p. 105) used field-recorded polysomnography in 80 truck drivers in the U.S. and
Canada, each studied for 5 nights. Overall, drivers obtained an average of only 4.8 hours
of sleep, with figures ranging from 3.8–5.4 hours, depending upon the schedule worked.
It is noteworthy that these average sleep durations are very similar to those of the
laboratory CPSD studies discussed earlier. Not surprisingly, the Mitler study also revealed
evidence of sleepiness (and in two drivers, stage 1 sleep), even when the drivers were
traveling at more than 45 mph (72 km/h). Mercifully, there were no accidents. In a
Finnish survey study of 184 long-haul and 133 short-haul truck drivers, Hakkanen and
Summala (2000) found that “About 40% of the long-haul drivers and 21% of the short-haul
drivers reported having problems in staying alert on at least 20% of their drives. Over
20% of the long-haul drivers also reported having dozed off at least twice while driving.
Near misses due to dozing off had occurred in 17% of these drivers” (p. 1).
Page 15 of 24

Loss of situational awareness
Falling asleep at work is not the whole story, however. One can argue that the real-world
analogue of the PVT performance lapse and/or cognitive rigidity, found in the laboratory,
is the loss of situational awareness that can occur in individuals with insufficient sleep.
Tragic accidents and near misses seldom occur because an individual’s response time
slows down. Rather, they occur because the individual momentarily loses awareness of all
of the various facets of the situation that he or she is supposed to keep in mind. This loss
manifests itself in the operator no longer responding appropriately, or perhaps even
responding completely inappropriately, to the true situation. Thus, in hindsight it is clear
to the individual concerned that an error was made or an important feature of the
situation was missed. Sometimes this loss of situational awareness results in a
catastrophe such as Three Mile Island or the Exxon Valdez (Mitler et al., 1988); at other
times the situation is saved by additional levels of safety control, resulting in only a near
miss.
In a recent publication (Monk, 2007), we discuss the issue of fatigue-related loss of

situational awareness, describing a 2007 public letter from Mark Rosenker, who was at
that time the chairman of the U.S. National Transportation Safety Board (NTSB), which
gave a useful insight into such real-world examples. The NTSB letter discussed one
recent catastrophe and four recent near misses in the field of commercial aviation that
may have resulted from a loss of situational awareness related to fatigue. In the
beginning of his letter, Chairman Rosenker discussed a 2006 fatal air crash at Kentucky:
“The airplane had been cleared by air traffic control (ATC) for takeoff on runway 22,
which is 7,003 feet long and equipped with high-intensity runway lights; however, the
crew mistakenly taxied onto runway 26, which is 3,500 feet long and unlighted, and
attempted to take off. The airplane ran off the end of runway 26, impacted the airport
perimeter fence and trees, and crashed. Of the 47 passengers and 3 crew members on
board the airplane, 49 were killed, and one received serious injuries […] During its
ongoing investigation of this accident, the Safety Board has learned that the air traffic
controller who cleared the accident airplane for takeoff had worked a shift from 0630 to
1430 the day before the accident, then returned (p. 106) 9 hours later to work the
accident shift from 2330 until the time of the accident at 0607 the next morning. The
controller stated that his only sleep in the 24 hours before the accident was a 2-hour nap
the previous afternoon between these two shifts.”
The NTSB chairman also gave four examples of near misses from Chicago (in 2006), Los
Angeles (in 2004), Denver (in 2001), and Seattle (in 2001), all potentially involving
fatigued air traffic controllers. In all four cases, a loss of situational awareness may have
been to blame. In three cases the air traffic controller put two planes on a collision course
on the same runway; in the fourth the controller failed to notice that the pilot had
selected the wrong runway (which was closed for repair). It is probably no coincidence
that all five of the incidents occurred immediately after a “short return,” i.e., a break of
only 9 hours between the end of one shift and the start of another. Short returns have
Page 16 of 24

been cited as the major problem with regard to backward (phase advance) rotating shifts
(Barton & Folkard, 1993), which are often a feature of U.S. ATC personnel shift systems.
There are two essential elements to the short-return problem. First is the fact that a 9-
hour break, even with minimal hand-off time, a short commute, and the minimum of time
spent unwinding, bathing, dressing and eating, can never allow an individual more than
about 5 or 6 hours of actual sleep. Second, there is the fact that the 9-hour break often
occurs during daylight hours, when both circadian biology and the surrounding
environment are resolutely opposed to an individual obtaining a restful bout of sleep,
even if sufficient time were available.
Page 17 of 24

Medical errors resulting from fatigue
While the air crashes and near misses are certainly disturbing, they pale in comparison to
the deaths and injuries that occur in hospitals because tired doctors and nurses make
cognitive errors. Every month the equivalent of about 58 jumbo jets full of passengers die
because of human errors made in America’s hospitals (The Washington Post, Monday,
April 2, 2007, http://www.washingtonpost.com/wp-dyn/content/article/2007/04/02/
AR2007040200813.html). Even if only 20% of these can be attributed to fatigue (a very
modest estimate), this still leaves the equivalent of the entire passenger complement of
more than 120 jumbo jets dying every year because of fatigue-related errors in U.S.
hospitals. Fortunately, the issue of medical house staff fatigue is no longer being swept
under the rug. Although the movement has taken a couple of decades to get going, there
are now many empirical studies and surveys that show that tired doctors, like tired air
traffic controllers, do indeed make errors. In the U.S., rules regarding work hours of
medical residents are now imposed. As reported by Philibert (2005) in July 2003, the U.S.
Accreditation Council for Graduate Medical Education (ACGME) instituted minimum
duty-hour standards for approximately 100,000 residents training in accredited programs
in the United States. The common minimum ACGME standards encompass an 80-hour
weekly limit and a limit of 24 hours on continuous duty, with an added period of up to 6
hours for the transfer of care and didactic activities. The fact that these “limits” are so
generous (and that even then, howls of protest from the medical establishment still
ensued) bespeaks the horrendous hours of duty that have hitherto been common and
accepted in the medical profession. Other countries have also started to crack down on
excessive work hours for doctors in training. In the European Union, for example, as of
August 2009, all hospital doctors were required to conform to the European Working
Time Directive (EWTD), which mandates that work rotas be based on a 48-hour
workweek (with up to 60 hours allowed), with mandated rest periods both within and
between shifts. Thus, there must be 11 hours of continuous rest per 24 hours, at least 24
hours of continuous rest out of each 7 days, and 45 minutes of rest per work shift.
Importantly, much of the empirical evidence that provided the impetus for the new rules
regarding work hours came from real doctors doing real medical tasks, thus weakening
the argument that somehow the practice of medicine is removed from the limitations of
the practitioner’s biology, and that the results from non-physicians doing laboratory tasks
do not apply. Thus, for example: in surgery, 20% more errors occurred and 14% more
time was required to perform simulated laparoscopy post-call (Taffinder et al., 1998;
Grantcharov et al., 2001); in internal medicine, the efficiency and accuracy of ECG
interpretation was impaired in sleep-deprived interns (Lingenfelser et al., 1994); in
anesthesiology, more than 60% of anesthesiologists report making fatigue-related errors
(Gravenstein et al., 1990); and in pediatrics, the time required to place an intra-arterial
line increased significantly in sleep-deprived pediatricians (Storer et al., 1989). In his
recent meta-analysis of published studies involving almost a thousand physicians,
Page 18 of 24

Philibert (2005) found that “Sleep loss of less than 30 hours reduced physicians’ overall
performance by nearly 1 standard deviation (p. 107) and clinical performance by more
than 1.5 standard deviations” (p. 1392).
Countermeasures
The main countermeasure to performance decrements resulting from sleep loss is the
obvious one of getting more sleep. However, this solution may be impacted by situational
and operational issues that can limit that extra sleep to a brief nap. Then, because sleep
inertia can itself negatively affect performance (see above), the use of a nap may, in some
cases, be counterproductive. As we have noted earlier, Wertz et al. (2006) have shown
that performance within 30 minutes of waking up may be as compromised as it is with 36
hours of TSD. However, more than 30 minutes after wake-up, depending upon individual-
difference and circadian issues relating to sleep inertia susceptibility (Silva & Duffy,
2008), the performance benefits from the sleep obtained in the nap will likely outweigh
the costs.
In an extended (56-hour) TSD experiment, Dinges and colleagues (Dinges et al., 1987)
showed that a 2-hour daytime nap before the 56-hour TSD had even started still led to
better performance throughout the TSD as compared to those not getting that nap. In an
extremely thorough study of the issue of “at work” naps in an operational air transport
setting, NASA researchers (Rosekind et al., 1994)(available at http://human-
factors.arc.nasa.gov/zteam/fcp/pubs/CRS.html) developed a standard protocol for
eliminating sleep inertia effects, and with that protocol in place showed that a 40-minute
nap in the cockpit significantly improved not only subjective and objective measures of
pilot alertness, but also actual performance indices related to the skill with which they
landed the airplane after a long-haul flight. Thus, if sleep inertia effects are not an issue,
or can be countered by, for example, the NASA protocol, then naps do undoubtedly
represent a worthwhile countermeasure to maintain good performance. Some companies
now have “alertness recovery rooms” where controlled napping is allowed during the
night shift. Also, advice to shift workers about to start a run of night duty, or an air
traveler about to undergo an overnight flight, may include the advice to take a
prophylactic nap on the day before (Monk, 2009). As we have discussed in relation to
siesta naps, afternoon placement of that nap (when feasible) can make use of the early
afternoon open “gate to sleep” to facilitate sleep onset.
The question then arises as to whether even the briefest of naps (sometimes called
“power naps”) can help. Opinion is divided as to whether such naps really help in
maintaining performance (Horne, 1988). Although not supported directly by empirical
study, the present author believes that there may be strong interindividual differences in
power nap efficacy, with some individuals benefiting and others worse off from having
that brief nap. These interindividual differences may possibly be parallel to those found in
Page 19 of 24

susceptibility to sleep deprivation (Van Dongen, 2006) and/or the presence of particular
genetic markers (Viola et al., 2007). Further research is clearly needed to elaborate the
individual-difference and genetic underpinnings of nap-related performance recovery.
Conclusions
The link between sleep and performance is profound, with important practical
ramifications. Alertness and performance impairments precede and follow the nocturnal
sleep period and can appear in the “siesta nap” interval during the day. Sleep deprivation
performance impairment can result from performance lapses, cognitive rigidity, cognitive
slowing, and motivation loss, with the particular pathway being dependent upon the task,
the individual, and the situation. Partial sleep deprivation leads to a progressive
impairment of alertness and performance as the week progresses. There is a need for
society to recognize the importance of obtaining sufficient sleep in order for people to
perform safely and productively.
Future directions
Can pharmacology ever provide long-term solutions to the problem of performance

impairment following chronic partial sleep loss?
Will it be possible to identify individuals a priori who will be particularly vulnerable to

performance impairment following sleep loss?
What behavioral and environmental countermeasures are the most effective in ensuring
good performance under conditions of sleep loss?
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The Role of Sleep in Neurocognitive Function

Matthew P. Walker

As critical as waking brain function is to cognition, an extensive literature now indicates

that sleep supports equally important, different, yet complementary operations. This
chapter first considers evidence for the role of sleep in memory processing, principally
focusing on declarative memory. Second, at a neural level, several mechanistic models of
sleep-dependent plasticity underlying these effects will be reviewed, with a synthesis of
these features offered that may explain the ordered structure of sleep and the orderly
evolution of memory stages. Third, accumulating evidence for the role of sleep in
associative memory processing will be discussed, suggesting that the long-term goal of
sleep may not be the strengthening of individual memory items, but instead their
abstracted assimilation into a schema of generalized knowledge. Finally, the newly
emerging benefit of sleep in regulating affective brain reactivity will be considered,
leading to a framework of sleep-dependent emotional processing.
Keywords: Learning, Memory, Encoding, Consolidation, Integration, Plasticity, Emotion, Affect, EEG, fMRI
“If sleep does not serve an absolutely vital function, then it is the biggest mistake
the evolutionary process has ever made”
Allan Rechtschaffen
University of Chicago Sleep Laboratory
Smithsonian, November 1978
Page 1 of 37
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Subscriber: University of Edinburgh; date: 14 May 2018

Introduction
A perplexing question continues to elude scientific judgment: “Why do we sleep?” In
accepting the utility of evolution, and as candidly stated by pioneering sleep researcher
Allan Rechtschaffen, sleep is likely to support some fundamental need of the organism.
Yet, despite the vast amount of time this state takes from our lives, we still lack any
consensus function for sleep. In part, this is undoubtedly because sleep, like its
counterpart wakefulness, serves not one but many functions, for brain and body alike.
Centrally, sleep is a brain phenomenon, and over the past 20 years an exciting
renaissance has taken place within the neurosciences, focusing on the question of why we
sleep, and specifically targeting the role of sleep in a number of cognitive and emotional
processes. This review aims to provide a synthesis of these recent findings in humans,
with the goal of extracting consistent themes across domains of brain function that
appear to be regulated by sleep. Providing a mechanistic foundation on which to consider
these findings, section I will briefly summarize the brain substrates of sleep—its
neurochemistry, neurophysiology, and functional anatomy. Section II will explore the role
of sleep in memory and brain plasticity and also examine competing models of sleep-
dependent learning. Section III will address the role of sleep beyond memory
consolidation, in processes of association, integration, and creativity. Finally, section IV
will discuss the more (p. 111) recent emerging role for sleep in emotional and affective
brain regulation.
Page 2 of 37

Sleep neurobiology
The sleep of mammalian species has been broadly classified into two distinct types; non-
rapid eye movement (NREM) sleep and rapid eye movement (REM) sleep, with NREM
sleep being further divided in primates and cats into 4 substages (1–4) corresponding, in
that order, to increasing depth of sleep (Rechtschaffen & Kales, 1968). In humans, NREM
and REM sleep alternate, or “cycle,” across the night in an ultradian pattern every 90
minutes (Figure 6.1). Although this NREM–REM cycle length remains largely stable
across the night, the ratio of NREM to REM within each 90-minute cycle changes, so that
early in the night stages 3 and 4 of NREM dominate, while stage 2 NREM and REM sleep
prevail in the latter half of the night. Interestingly, the functional reasons for this
organizing principal (deep NREM early in the night, stage 2 NREM and REM late in the
night) remains unknown—another perplexing mystery of sleep.
As NREM sleep progresses, electroencephalographic (EEG) activity begins to slow in

frequency. Throughout stage 2 NREM, there is the presence of phasic electrical events
including K-complexes (large electrical sharp waves in the EEG) and sleep spindles (short
synchronized 10–16 Hz) EEG oscillations (Steriade & Amzica, 1998). The deepest stages
of NREM, stages 3 and 4, are often grouped together under the term “slow-wave
sleep” (SWS), reflecting the occurrence of low-frequency waves (1–4 Hz and below <1
Hz), which have themselves been termed slow-wave activity (SWA), representing an
expression of underlying mass cortical synchrony (Amzica & Steriade, 1995). During REM
sleep, however, EEG wave forms once again change in their composition, associated with
oscillatory activity in the theta band range (4–7 Hz), together with higher frequency
synchronous activity in the 30–80 Hz range (“gamma”) (Llinas & Ribary, 1993; Steriade,
Amzica, & Contreras, 1996). Periodic bursts of rapid eye movement also take place, a
defining characteristic of REM sleep, associated with the occurrence of phasic
endogenous wave forms expressed in, among other regions, the pons (P), the lateral
geniculate nuclei of the thalamus (G), and the occipital cortex (O), and as such have been
termed “PGO waves” (Callaway, Lydic, Baghdoyan, & Hobson, 1987).
As the brain passes through these sleep stages, it also undergoes dramatic alterations in
neurochemistry. In NREM sleep, subcortical cholinergic systems in the brainstem and
forebrain become markedly less active (Hobson, McCarley, & Wyzinski, 1975; Lydic &
Baghdoyan, 1988) while firing rates of serotonergic raphe neurons and noradrenergic
locus coeruleus neurons are also reduced relative to waking levels (Aston-Jones & Bloom,
1981; Shima, Nakahama, & Yamamoto, 1986). During REM sleep, both these aminergic
populations are strongly inhibited while cholinergic systems become as/more active
compared to wake (Kametani & Kawamura, 1990; Marrosu et al., 1995), resulting in a
brain state largely devoid of aminergic modulation and dominated by acetylcholine.
Page 3 of 37

At a whole-brain systems
level, neuroimaging
techniques have revealed
complex and dramatically
different patterns of
functional anatomy
associated (p. 112) with
Fig. 6.1 The human sleep cycle. Across the night,
NREM and REM sleep cycle every 90 minutes in an NREM and REM sleep (for
ultradian manner, while the ratio of NREM to REM review, see Nofzinger,
sleep shifts. During the first half of the night, NREM
stages 3 and 4 NREM (SWS) dominate, while stage 2
2005). During NREM SWS,
NREM and REM sleep prevail in the latter half of the rostral brainstem regions,
night. EEG patterns also differ significantly between
thalamic nuclei, basal
sleep stages, with electrical oscillations such as slow
delta waves developing in SWS, K-complexes and ganglia, hypothalamus,
sleep spindles occurring during stage 2 NREM, and prefrontal cortex,
theta waves seen during REM.
cingulate cortices, and
medial regions of the
temporal lobe all appear to undergo reduced activity. However, during REM sleep,
significant elevations in activity have been reported in the pontine tegmentum, thalamic
nuclei, occipital cortex, mediobasal prefrontal lobes, and associated limbic groups
including the amygdala, hippocampus, and anterior cingulate cortex. In contrast, the
dorsolateral prefrontal cortex, posterior cingulate, and parietal cortex appear least active
in REM sleep.
Although this summary only begins to describe the range of neural processes that are
affected by the brain’s daily transit through sleep states, it clearly demonstrates that
sleep itself cannot be treated as a homogeneous entity, which may or may not regulate
cognitive processes. Instead, this constellation of sleep stages offers a range of distinct
neurobiological mechanisms that can potentially support the modulation, regulation, and
preparation of numerous brain functions.
Memory processing and brain plasticity
When considering the role of sleep in memory processing, it is pertinent to appreciate

that memories evolve (Walker & Stickgold, 2006). Specifically, memories pass through
discrete stages in their “life span.” The conception of a memory begins with the process
of encoding, resulting in a stored representation of an experience within the brain (Paller
& Wagner, 2002). However, it is now understood that a vast number of post-encoding
memory processes can take place (Stickgold & Walker, 2005). For memories to persist
over the longer time course of minutes to years, an offline, nonconscious operation of
consolidation appears to be necessary, affording memories greater resistance to decay (a
process of stabilization), or even improved recollection (a process of enhancement)
(Robertson, Pascual-Leone, & Miall, 2004; Walker, 2005). Sleep has been implicated in
both the encoding and consolidation of memory.
Page 4 of 37

Sleep And Memory Encoding

One of the earliest human studies to report the effects of sleep and sleep deprivation on
declarative memory encoding was by Morris et al. (Morris, Williams, & Lubin, 1960),
indicating that “temporal memory” (memory for when events occur) was significantly
disrupted by a night of pre-training sleep loss. These findings have been revisited in a
more rigorous study by Harrison and Horne (2000), again using the temporal memory
paradigm. Significant impairments in retention were evident in a group of subjects
deprived of sleep for 36 hours, scoring significantly lower than controls, even in a
subgroup that received caffeine to overcome nonspecific effects of lower arousal.
Furthermore, the sleep-deprived subjects displayed significantly worse insight into their
memory encoding performance, resulting in lower predictive ability of performance.
Pioneering work by Drummond and colleagues has examined the neural basis of similar
memory impairments using fMRI, investigating the effects of 35 hours of total sleep
deprivation on verbal learning (Drummond et al., 2000). In those who were sleep
deprived, regions of the medial temporal lobe were significantly less active during
learning relative to a control group that had slept, while the prefrontal cortex actually
expressed greater activation. Most interesting, the parietal lobes, which were not
activated in the control group during learning, were significantly active in the deprivation
group. Such findings suggest that inadequate sleep (at least following one night) prior to
learning produces bidirectional changes in episodic encoding activity, involving the
inability of the medial temporal lobe to engage normally during learning, combined with
potential compensation attempts by prefrontal regions, which in turn may facilitate
recruitment of parietal lobe function (Drummond & Brown, 2001).
The impact of sleep

deprivation on memory
formation may be
especially pronounced for
emotional material. We
have investigated the
impact of sleep deprivation
Click to view larger on the encoding of
Fig. 6.2 Sleep deprivation and encoding of emotional emotionally negative,
and non-emotional declarative memory. Effects of 38 positive, and neutral words
hr of total sleep deprivation on encoding of human
declarative memory (A) when combined across all
(Walker, unpublished
emotional and non-emotional categories; (B) when results). When combined
separated by emotional (positive and negative
across all stimulus types,
valence) and non-emotional (neutral valance)
categories. subjects in the sleep-
†p < 0.08, *p < 0.05, **p < 0.01, error bars deprived condition
represent s.e.m. exhibited a striking 40%
reduction in the ability to
form new human memories under conditions of sleep deprivation (Figure 6.2A). However,
when these data were separated into the three affective categories (negative, positive, or
Page 5 of 37

neutral), the magnitude of encoding impairment differed (Figure 6.2B). In those that had
slept, both positive and negative stimuli were associated with superior retention levels
relative the neutral condition, consonant with the notion that emotion facilitates memory
encoding (Phelps, 2004). However, there was severe disruption of encoding and hence
later retention for neutral and especially positive emotional memory in the sleep-deprived
group. In contrast, a relative (p. 113) resistance of negative emotional memory was
observed in the deprivation group. These data suggest that, while the effects of sleep
deprivation are directionally consistent across memory subcategories, the most profound
impact is on the encoding of positive emotional stimuli and, to a lesser degree,
emotionally neutral stimuli. In contrast, the encoding of negative memory appears to be
more resistant to the effects of prior sleep loss, at least following one night.
Intriguingly, these data may offer novel insights into affective mood disorders that
express co-occurring sleep abnormalities (Benca, Obermeyer, Thisted, & Gillin, 1992;
Buysse, 2004). Indeed, if one compares the profiles of memory encoding in Figure 6.2B, it
is clear that those who have slept encode and retain a balanced mix of both positive and
negative memories. In contrast, however, those who have not slept display a skewed
relative distribution of encoding, resulting in an overriding dominance of negative
memories, combined with a marked retention deficit of positive and neutral memories.
This selective alteration in memory encoding may provide an experimental explanation
for the higher incidence of depression in populations that suffer sleep disruption (Buysse,
2004; Shaffery, Hoffmann, & Armitage, 2003), which, due to these specific deficits, may
impose a negative remembering bias, despite experiencing equally positive and negative
reinforcing event histories.
The impact of sleep deprivation on the neural dynamics associated with declarative
memory encoding has recently been examined using event-related fMRI (Yoo, Gujar, Hu,
Jolesz, & Walker, 2007). In addition to performance impairments under condition of sleep
deprivation, and relative to a control group that slept, a highly significant and selective
deficit was identified in bilateral regions of the hippocampus—a structure known to be
critical for learning new episodic information (Eichenbaum, 2004). While these findings
indicated that, at a group level, sleep deprivation markedly impairs hippocampal memory
function, when examined within each group separately the success of encoding, from low
to high, was further associated with activity in different regions of the prefrontal lobe. In
those that had slept prior to learning, the right dorsal/middle lateral prefrontal cortex
showed a strong positive relationship with the proficiency of memory encoding. In
contrast, a region in the right inferior frontal gyrus (IFG) displayed a significant positive,
potentially compensatory relationship with memory performance in those who were sleep
deprived.
Taken together, this collection of findings indicates the critical need for sleep before
learning in preparing key neural structures for efficient next-day learning. Without
adequate sleep, hippocampal function becomes markedly disrupted, resulting in the
Page 6 of 37

decreased ability for recording new experiences, the extent of which appears to be
further governed by alterations in prefrontal encoding dynamics.
Page 7 of 37

Sleep And Memory Consolidation

Using a variety of behavioral paradigms, evidence for the role of sleep in memory
consolidation has now been reported across a diverse range of phylogeny. (p. 114)
Perhaps the earliest recorded evidence for the role of sleep in human memory processing
is by researchers such as David Hartley (1801) and Jenkins and Dallenback (1924),
indicating that the strength of a memory may be more preserved by periods of sleep than
equivalent periods of time awake. Following the discovery of discrete sleep stages
(Aserinsky & Kleitman, 1953), research investigating the influence of sleep on memory
has become gradually more complex at both a behavioral and mechanistic level. A robust
and consistent literature has demonstrated the need for sleep after learning in the
subsequent consolidation and enhancement of procedural memories, the evidence for
which has recently been reviewed elsewhere (Walker & Stickgold, 2006). Early work
focusing on the role for sleep in declarative memory processing was somewhat less
consistent, but more recent findings have now begun to reveal a robust beneficial effect
of sleep on the consolidation of declarative memory—our focus here (Ellenbogen, Payne,
& Stickgold, 2006; Smith, 2001; Walker & Stickgold, 2006).
Several reports by Born and his colleagues have shown offline improvement on a word-
pair association task following sleep, attributed to early night sleep rich in SWS (Gais &
Born, 2004; Plihal & Born, 1997, 1999). More recently, the same group has demonstrated
that, in addition to classically defined slow delta waves (0.5–4 Hz), the very slow cortical
oscillation (< 1 Hz) appears to be important for the consolidation of declarative
memories. Following learning of a word-pair list, a technique called “direct current
stimulation” was used to induce slow oscillation-like field potentials in the prefrontal
cortex (in this case at 0.75 Hz) during early night SWS (Marshall, Helgadottir, Molle, &
Born, 2006). Direct current stimulation not only increased the amount of slow oscillations
during the simulation period (and for some time after), but also enhanced next-day word-
pair retention, suggesting a causal benefit of SWS neurophysiology for the offline
consolidation of episodic facts.
Rather than simply testing memory recall, Ellenbogen and colleagues have since revealed
the extent of sleep’s ability to protect declarative memories using experimentally induced
learning disruption (Ellenbogen, Hulbert, Stickgold, Dinges, & Thompson-Schill, 2006).
Taking advantage of a classic interference technique called the A-B–A-C paradigm,
subjects first learned unrelated word-paired associates, designated as list A-B (e.g., leaf-
wheel). After sleep at night, or wakefulness during the day, half of the subjects in each
group learned a new, interfering list containing a new associate paired with the first
word, designated as list A-C (e.g., leaf-nail), before being tested on the original A-B list
(e.g., leaf-wheel). In the groups that did not experience the interfering challenge—simply
being trained and then tested on list A-B—sleep provided a modest benefit to memory
recollection (Figure 6.3A). However, when testing the groups that were exposed to
interfering list learning (list A-C) prior to recalling the original list (list A-B), a large and
significant protective benefit was seen in those that slept (Figure 6.3B). Thus, memories
tested after a night of sleep were significantly more resistant to interference, whereas
Page 8 of 37

across a waking day, memories were far more susceptible to this antagonistic learning
challenge. Yet, it was only by using an interfering challenge, the A-C list, that the true
benefit of sleep’s protection of memory was revealed—a benefit that would not
necessarily have been evident in a standard study-test memory paradigm.
One mechanism proposed to underlie these effects on hippocampal-dependent learning

tasks (see next section) is the reactivation of memory representations at night. A
considerable number of reports have investigated the firing patterns of large networks of
individual neurons across the wake–sleep cycle in animals. The signature firing patterns
of these hippocampal and cortical networks, expressed during waking performance of
spatial tasks and novel experiences, appear to be “replayed” during subsequent SWS
(and, in some studies, also REM) (Dave & Margoliash, 2000; Dave, Yu, & Margoliash,
1998; Ji & Wilson, 2007; Jones & Wilson, 2005; Louie & Wilson, 2001; Poe, Nitz,
McNaughton, & Barnes, 2000; Ribeiro et al., 2004; Skaggs & McNaughton, 1996; Wilson
& McNaughton, 1994). Homologous evidence has been reported in the human brain using
a virtual maze task in combination with positron-emission tomography (PET) scanning.
Daytime learning was initially associated with hippocampal activity. Then, during post-
training sleep, there was a re-emergence of hippocampal activation, specifically during
SWS. Most compelling, however, the amount of SWS reactivation in the hippocampus was
proportional to the amount of next-day task improvement, suggesting that this
reactivation is associated with offline memory improvement (Peigneux et al., 2004).
Page 9 of 37

Building on the framework

Fig. 6.3 Neural basis of sleep-deprivation induced
encoding deficits. (A) Regions (circled) of decreased
that memories,
encoding activation in the sleep deprivation group
relative to the sleep control group in bilateral particularly those
involving the
posterior hippocampus, together with a histogram of
parameter estimates (effect size) of averaged
hippocampus, are
hippocampal activity in each group. Effects are
reactivated at night during
significant at P < 0.001; >5 contiguous voxels. (B)
Correlation analysis with memory performance sleep, Rasch et al. have
showing regions of significant association between
encoding-related activation and memory taken advantage of the
classical psychology effect
performance (d’) across subjects in the sleep control
group (peak - right Middle/dorso-lateral prefrontal
of (p. 115) cue-dependent
cortex), and (C) in the sleep deprivation group (peak
- right Inferior frontal gyrus). recall and translated it into
a sleep-dependent
consolidation paradigm (Rasch, Buchel, Gais, & Born, 2007). It is well known that
memory can be strongly modulated by smell (Cann & Ross, 1989); most of us have
associated the smell of a certain perfume or cologne with a particular person, and when
we encounter that same perfume again, it often results in the powerful cued recall of
memories of that particular person. In this study, however, following learning of a spatial
memory task that was paired with the smell of rose, the odor was not re-presented again
at retrieval, but instead during subsequent SWS that night—a time when consolidation
was presumed to be occurring. Relative to a control condition where the odor was not
presented again during SWS, the re-perfusion of the rose scent at night resulted in
significantly improved recall the following day. Moreover, the re-presentation of the odor
resulted in greater reactivation of the hippocampus during SWS. These findings support
the role of SWS in the consolidation of individual declarative memories and suggest that
an active reprocessing of hippocampal-bound information may take place during SWS.
(p. 116)
Models Of Sleep-Dependent Memory Processing

Elucidating the neural mechanisms that control and promote sleep-dependent human
memory consolidation remains an active topic of research and debate (Miller, 2007). It is
perhaps unlikely that multiple different memory systems, involving diverse cortical and/or
subcortical networks, require the same underlying neural mechanisms for their
modulation. Even if they do, it is not clear that this process would rely on just one type of
sleep-stage physiology (Giuditta et al., 1995). At present, two intriguing models of sleep-
dependent plasticity, relevant to declarative memory, have been offered to account for the
overnight facilitation of recall, which build on different aspects of neural activity during
sleep: 1) hippocampal-neocortical dialogue and 2) synaptic homeostasis hypothesis.
Hippocampal-neocortical dialogue
Page 10 of 37

There is considerable
agreement that structures
within the medial temporal
lobe (MTL), most notably
the hippocampal complex,
are crucial for the
formation and retrieval of
new declarative memories.
These structures are
believed to guide the
reinstatement of recently
formed memories by
binding together patterns
of cortical activation that
were present at the time of
initial learning. A classical
Fig. 6.4 Impact of sleep on the consolidation and
stabilization of declarative memory. Percent correct model of declarative
recall for B words from the original A-B pair after a memory consolidation
12 hr retention interval of either wake or sleep
following no interference or interference learning suggests that information
(list A-C). †p < 0.10, *p < 0.05, **p < 0.001; error initially requires MTL
bars indicate s.e.m. Modified from Ellenbogen et al.
binding, but over time, and
(2007a).
by way of slow offline
processes, is eventually
integrated into neocortical circuits (Figure 6.4). Neocortical structures thus become the
eventual storage site for consolidated episodic memories through cross-cortical
connections, and, as a consequence, the MTL is not necessary for their retrieval.
Therefore, the classical model of memory consolidation holds that neocortical structures
become increasingly important for the retention and retrieval of successfully consolidated
episodic memories, while the corresponding contribution of the hippocampus
progressively decreases (McClelland, McNaughton, & O’Reilly, 1995; Squire, 1992, 2004;
Squire & Zola, 1996). It should be noted, however, that controversy remains about the
role of these MTL structures in the retrieval of declarative memories after the passage of
time. This has led to the emergence of alternate consolidation models, most notably
Nadel and Moscovitch’s “multiple trace theory” (Moscovitch & Nadel, 1998; Nadel &
Moscovitch, 1997), which posits that hippocampal involvement is always critical for the
retrieval of episodic (but not semantic) memories, and that these memories remain
permanently dependent on hippocampal-neocortical connections (for discussion beyond
the scope of this review, see Frankland & Bontempi, 2005).
In addition to its role in binding distributed cortical memory components, Marr and later
McClelland and colleagues suggested that the hippocampus plays a critical role in
reactivating these networks, specifically during sleep (Marr, 1970; McClelland et al.,
1995). This process of reactivation would, over multiple sleep cycles across a night and/or
multiple occurrences of sleep over many nights, gradually strengthen the initially weak
Page 11 of 37

connections between neocortical sites, thereby reinforcing them (Figure 6.4). Eventually,
this strengthening would allow the original information to be activated in the cortex,
independent of the hippocampus. Buzsaki (1996) has since advanced on these ideas,
proposing a model of consolidation that involves two stages or states of hippocampal
activity, the first involving a mode of “recording” during wake, which shifts to a
“playback” mode during NREM SWS, (p. 117) specifically during bursts of neural activity
called sharp-waves.
Interestingly, this model makes two predictions about the impact of sleep on declarative
memory. The first is that declarative memories from the day prior should be more
resistant to interference the next day due to the increased cortico-cortical connections
formed during overnight consolidation (Figure 6.4). It is precisely this behavioral effect
that was reported in the study by Ellenbogen et al., showing greater post-sleep resistance
to interference, using the A-B–A-C paradigm (Ellenbogen, Hulbert, et al., 2006). A second
and far less considered benefit of this sleep-dependent dialogue is the encoding capacity
of the hippocampus (Figure 6.4). If the strengthening of cortico-cortical connections takes
place during sleep, albeit iteratively, then blocking sleep after hippocampal learning
should negate this offline transfer, preventing the development of independence from (or
“refreshing” of) the hippocampus, and by doing so decrease the capacity for new
hippocampal learning the next day. This second premise appears to accurately explain the
findings discussed in the memory encoding section above (Yoo, Hu, Gujar, Jolesz, &
Walker, 2007), which describe a significant impairment of hippocampal encoding activity
when sleep has not taken place (deprivation), associated with a decreased ability to form
new episodic memories.
Two recent reports have provided early evidence in support of this sleep-dependent
dialogue and neural transformation of declarative memory. In the first such report,
Takashima and colleagues examined the benefit of daytime naps on episodic declarative
memory consolidation (Takashima et al., 2006). In addition to a long-term evaluation of
memory over 3 months, there was also a short-term evaluation of memory across the first
day, which included a intervening nap period (90 minutes) between training and testing of
the original studied (“remote”) stimuli. Interestingly, the duration of NREM SWS during
the intervening nap correlated positively with later recognition memory performance, yet
negatively with retrieval-related activity in the hippocampus.
Furthermore, with increasing time following learning, there was progressively greater
recall activity in medial prefrontal regions, and a continued dissipation of retrieval-
related activity within the hippocampus. Advancing on these findings, Maquet and
colleagues have since demonstrated that one night of post-training sleep deprivation,
even following recovery sleep, significantly impairs the normal modulation of
hippocampal activity associated with episodic memory recollection (Gais et al., 2007).
Furthermore, first-night sleep deprivation also prevented an increase in hippocampal
connectivity with the medial prefrontal cortex, a development that was observed only in
those who sleep after learning.
Page 12 of 37

While no one study has yet demonstrated that the neural signature of learning during the
day is subsequently reactivated and driven by characteristics of SWS at night, and that
the extent of these properties are consequently proportional to the degree of next-day
recall and memory reorganization, collectively they offer a persuasive foundation on
which to entertain this possibility.
Synaptic homeostasis hypothesis

In recent years, an orthogonal theory of SWS and learning has emerged that postulates a
role for sleep in regulating the synaptic connectivity of the brain—principally the
neocortex (Tononi & Cirelli, 2003, 2006). The model by Tononi and Cirelli considers
NREM SWS, and specifically the magnitude of slow-wave activity (SWA) of SWS, as a
brain state that promotes the decrease of synaptic connections, not their increase.
Accordingly, plastic processes, such as learning and memory occurring during
wakefulness, result in a net increase in synaptic strength in diffuse brain circuits. The
role of SWS, therefore, and the slow oscillation in particular, is to selectively downscale
or “depotentiate” synaptic strength back to baseline levels, preventing synaptic over-
potentiation, which would result in saturated brain plasticity. In doing so, this re-scaling
would leave behind more efficient and refined memory representations the next day,
affording improved recall.
A number of human studies by Huber, Tononi, and colleagues have provided evidence
supporting their model. For example, it has been shown that learning of a motor skill
adaptation task during the day subsequently triggers locally specific increases in cortical
SWA at night, the extent of which is proportional to both the amount of initial daytime
learning and the degree of next-day improvement (Huber, Ghilardi, Massimini, & Tononi,
2004). Furthermore, experimentally impairing the amount of experience-dependent
activity during the day (arm immobilization) produced the opposite effect—reduced
amounts of SWA activity in associated cortical regions (Huber et al., 2006). These
findings substantiate the concept of local sleep-dependent neural pruning by SWS, the
goal (p. 118) of which may be to regulate neural architecture at a highly specific
anatomical level, mapping onto the corresponding location of the memory representation.
Interestingly, this model would similarly predict that sleep deprivation, specifically the
loss of SWS, would also negate effective new learning the next day, due to over-
potentiation of synaptic connections. Thus, any region that exhibits SWA and is involved
in representing memory (e.g., hippocampus) would display a corresponding inability to
code further information beyond a normal waking duration (∼16 hours in humans). Such
a premise may offer an alternative explanation to the marked hippocampal encoding
deficits reported under conditions of sleep loss (Yoo, Hu, et al., 2007).
Page 13 of 37

A role for sleep spindles?

Independent of both models, which consider the role of SWS in memory processing, a
number of reports have also described an association between learning and the hallmark
feature of stage 2 NREM: sleep-spindles—short (∼1-second) synchronous bursts of
activity expressed in the EEG in the 10–16 Hz frequency range (Sejnowski & Destexhe,
2000; Smith, Aubrey, & Peters, 2004; Steriade, 2001). For example, following learning of
a motor skill memory task Nishida and Walker (2007) have examined post-training spindle
activity over the motor cortex, evaluating the difference in spindle activity in the learning
hemisphere (since subjects performed the task with their left non-dominant hand),
relative to the non-learning hemisphere (Figure 6.5A). Remarkably, when sleep-spindle
power at electrode sites above the primary motor cortex of the non-learning hemisphere
(left) were subtracted from those in the learning hemisphere (right), representing the
within-subject, between-hemisphere difference in spindle activity following learning, a
strong predictive relationship with the amount of memory improvement emerged (Figures
6.5B & 6.5C). Similarly, Fogel, Jacob, and Smith (2001) have reported increased spindle
density after intensive training on a pursuit motor skill task, and Fogel and Smith (2006)
reported increased spindle density after combined training on several simple procedural
motor tasks.
Such findings, especially the former, indicate that the enhancement of specific memory
representations is associated with electrophysiological events expressed at local,
anatomically discrete locations of the brain. Contrasting with the proposed impact of
SWS, the mechanistic benefit of sleep spindles may be related to their faster stimulating
frequency, a range suggested to facilitate long-term potentiation (a foundational principal
of synaptic strengthening in the brain) (Sejnowski & Destexhe, 2000; C. T. Smith et al.,
2004; Steriade, 2001) and not synaptic depression. This increase in spindle activity may
represent a local, endogenous trigger of intrinsic synaptic plasticity, again corresponding
topographically to the underlying memory representation (Nishida & Walker, 2007).
Increases in post-training
spindle activity are not
limited to procedural
memory tasks. For
example, Gais et al. have
Click to view larger shown that, following
Fig. 6.5 Sleep spindles and motor-skill memory learning of a word-pair
plasticity. (A) Sleep-EEG array (blue discs)
superimposed on the known overnight plastic task, there is a
reorganization of motor memory, including the right concomitant increase in
motor cortex (red). (B) Difference in sleep-spindle
sleep spindle density,
activity (power) following task training in the
learning (relative to non-learning) hemisphere, which which correlates both with
(C) accurately predicts the amount of post-sleep the extent of prior learning
memory improvement across subjects. Modified from
Nishida and Walker (2007). and the proficiency of
memory recalled the next
day. These findings mirror previous observations by Meier-Koll et al. (Meier-Koll,
Page 14 of 37

Bussmann, Schmidt, & Neuschwander, 1999), (p. 119) who reported a similar increase in
spindles following learning of a hippocampally dependent maze task, and by Clemens et
al. (Clemens, Fabo, & Halasz, 2005) who found a correlation between spindle density and
overnight verbal memory retention (although not memory for faces).
Intriguingly, studies discussed above by Marshall et al. (2006) and Huber et al. (2004),
which implicate slow oscillatory activity associated with offline memory improvement,
also describe similar albeit near significant associations with activity in the sleep spindle
frequency range. There may be a combinatory role for spindles in regulating plasticity,
together with SWS.
Reconciling models
None of these models needs necessarily to be wrong. Instead, aspects of each may afford
complimentary and synergistically beneficial outcomes for memory. Clues to this
possibility lie within the ordered structure of human sleep (Figure 6.1), with NREM SWS
dominating early in the night and stage 2 NREM and REM prevailing later in the night.
When placed in this temporal framework, a progression of events emerges that may be
optimal for the neuroplastic modulation of memory representations. From a reactivation
perspective, the predominance of hippocampal-neocortical interaction would take place
in the early SWS-rich phase of the night, leaving cortico-cortical connections on offer for
later processing during stage 2 NREM and REM. Similarly, and even in coincidence, SWS
may downscale cortical (and possibly subcortical) plasticity, and do so in a learning-
dependent manner, again leaving only those representations which are strongest—
including those strengthened by hippocampal-neocortical interplay—for processing
during these latter periods of sleep, dominated by faster frequency oscillations.
This concept is analogous to the art of sculpture. During the day, through experience,
substantial informational “clay” is acquired on the cortical pedestal, some relevant, some
not. Once accumulated, the next step is to carve out and select the strongest and most
salient memory representations (“statues”) for the organisms—a mechanism that SWS,
occurring first and predominately early in the night, may be ideally suited for. Following
such down-scaling and/or dynamic selection of memory through translocation, the
remaining cortical representations—the rough outline of the sculpted form—may finally
be strengthened by faster frequency oscillations, including those of sleep spindles (and
potentially PGO-wave burst during REM (Datta, 2000; Datta, Li, & Auerbach, 2008), more
associated with the potentiation of synaptic connections, and not their de-potentiation.
This final step is akin to polishing and improving the detailed features of the memory
statue, which in terms of computational modeling would offer improved signal-to-noise
quality within the system. Such a cooperative mechanism, which appreciates the
temporal order of the wake–sleep cycle (acquisition, followed by post-processing), and
within sleep, the ultradian pattern of sleep-stage progression across a night (selection
and removal, followed by strengthening), would produce a network of stored information
that is not only more efficient, but for those representations remaining, more enhanced.
Both these processes would predict improved recall of remodeled individual memories
Page 15 of 37

from the prior day and further afford the synaptic capacity for efficient acquisition of new
“information clay” the next day.
Association, integration, and creativity
As critical as consolidation may be—an operation classically concerned with individual

memory items—the association and integration of new experience into pre-existing
networks of knowledge is equally, if not more, important. The resulting creation of
associative webs of information offers numerous and powerful advantages. Indeed, the
end goal of sleep-dependent memory processing may not be the enhancement of
individual memories in isolation, but instead their integration into a common schema, and
by doing so facilitate the development of universal concepts, a process that forms the
basis of generalized knowledge, and even creativity.
Association And Integration

Perhaps the earliest demonstration that sleep may be involved in a form of memory
generalization was by Fenn, Nusbaum, and Margoliash (2003). Utilizing an artificial
grammar task, subjects were trained and later tested on their ability to generalize
phonological categories across different acoustic patterns. The task required forming new
mappings from complex acoustical sounds to pre-existing linguistic categories, which
then generalized to new stimuli. As such, it involved both a declarative process of forming
specific memories associated with the learned stimuli, together with a procedural
component involving mapping across the set of learned sounds that supports
generalization to novel stimuli. During the initial training session there was a significant
improvement in recognition performance (p. 120) on the task. However, when retested
after a 12-hour waking interval, performance had decayed. Yet, if subjects were retested
following a night of sleep, this ability for memory generalization was restored.
In a related study by Gomez and colleagues (Gomez, Bootzin, & Nadel, 2006), infants
were exposed to “phrases” from an artificial language during a learning session—for
example, phrases like “pel–wadim–jic”—until the infants became familiar (as indexed by
look responses). However, these three syllable units had an embedded rule, which was
that the first and last unit formed a relationship of non-adjacency; in this case, pel
predicts jic. The infants were then retested several hours later, yet some infants took
normally scheduled naps, while others were scheduled at a time when they would not
sleep after learning. At later testing, infants again heard the recordings, along with novel
phrases in which the predictive relationship between the first and last word was new.
Infants who did not sleep recognized the phrases they had learned earlier, yet those who
had slept demonstrated a generalization of the predictive relationship to new phrases,
suggesting that the intervening process of sleep allowed the reinterpretation of prior
experience and supported the abstraction of commonalities—that is, the ability to detect a
general pattern in new information.
Page 16 of 37

Ellenbogen et al. have

since directly tested this
sleep-dependent
hypothesis of integration
by examining human
relational memory—
defined as the flexible
ability to generalize across
existing stores of
information. Participants
initially learned five
“premise pairs” (A>B,
B>C, C>D, D>E, E>F).
Unknown to subjects, the
pairs contained an
embedded hierarchy
Fig. 6.6 Sleep-dependent integration of human
relational memory. (A) Delayed inference (A>B>C>D>E>F).
(associative) memory performance (% correct) in a Following an offline delay
relational memory task following different offline
delays. Immediate testing after just a 20-min. offline of 20 minutes, 12 hours
delay demonstrated a lack of any inferential ability across the day, or 12 hours
resulting in chance performance on both 1-degree
containing a night of sleep,
(first order) and 2-degree (second order) associative
judgments. Following a more extended 12-hr delay, knowledge of this
across the day (wake group), performance was hierarchy was tested by
significantly above chance across both the one- and
two-degree inference judgments. However, following examining relational
an equivalent 12-hr offline delay, but containing a judgments for novel
night of sleep (sleep group), significantly better
“inference” pairs,
performance was expressed on the more distant two-
degree inference judgment compared with the one- separated by either 1
degree judgment. (B) A conceptual model of the degree of associative
effects of sleep on memory integration. Immediately
after learning, the representation of each premise is distance (B>D, C>E pairs)
constituted as the choice of one item over another (A or 2 degrees of associative
> B, etc.), and these premises are isolated from one
distance (B>E pair).
another despite having overlapping elements. After a
12-hr period with no sleep, the premise Despite all groups
representations are partially integrated by their achieving near-identical
overlapping elements, sufficient to support first-
order transitive inferences. However, following a 12- premise-pair retention
hr offline period with sleep, the premise after the offline delay (i.e.,
representations are fully interleaved, supporting
the building blocks of the
both first- and second-order transitive inferences.
hierarchy), a striking
*p < 0.05; error bars indicate s.e.m. Modified from
Ellenbogen et al. (2007b). dissociation was evident in
the ability to make
relational inference judgments. Subjects that were tested soon after learning in the 20-
minute group showed no evidence of inferential ability, performing at chance levels
(Figure 6.6A). In contrast, the 12-hour groups displayed highly significant relational
memory development. Most remarkable, however, was that if the 12-hour period
contained a night of sleep, a near 25% advantage in relational memory was seen for the
Page 17 of 37

most (p. 121) distantly connected inferential judgment (the B>E pair; Figure 6.6A).
Together, these findings demonstrate that human memory integration takes time to
develop, requiring slow, offline associative processes. Furthermore, sleep appears to
preferentially facilitate this integration by enhancing hierarchical memory binding,
biasing the development of the most distant/weak associative links amongst related yet
separate memory items (Figure 6.6B). It is also interesting to note a further advantage of
this sleep-dependent assimilation process. When stored as individual premise pairs (top
row, Figure 6.6B), the size/number of items (“bits”) of information to code is 10 (A-B, B-C,
C-D, D-E, E-F). However, when formed into a hierarchy, the informational load is
compressed, reduced by nearly 50% to just six bits (A-B-C-D-E-F). Therefore, a
supplementary benefit of sleep-dependent memory association may be the improved
efficiency of memory storage, in addition to a more useful and flexible representation.
Thus, the overnight strengthening and consolidation of individual item memories

(reviewed above), may not be the ultimate objective of sleep-dependent memory
processing, especially when considering that declarative (non-emotional) memories decay
over the long term (Wixted & Carpenter, 2007). It is then interesting to speculate whether
sleep serves to facilitate two complimentary objectives for declarative memory that span
different time courses. The first may be an initial process of consolidating individual item
(episodic) memories that are novel, which may occur in the relative short term. Over a
longer time course, however, and utilizing these recently consolidated item memories
prior to their fading, sleep may begin the process of extraction and abstraction, taking
veridical information and generalizing key aspects into more adaptive semantic networks.
Ultimately, the individual item memories would no longer be necessary for the goal that
sleep is trying to achieve, and only the conceptual meaning of such experiences would
remain—the difference between knowledge (remembering individual facts) and wisdom
(understanding what they all mean). Whether the subsequent loss of item memories is
passive, or whether sleep plays an active role in this process (Crick & Mitchison, 1983),
remains to be examined, but this is a testable hypothesis, i.e., forgetting (individual items)
is the price we pay for remembering (general rules).
Creativity
One potential advantage of testing associative connections and building cross-linked
systems of knowledge is creativity—the ability to take existing pieces of information and
combine them in novel ways that lead to greater understanding and offer new
advantageous behavioral repertoires. The link between creativity and sleep, especially
dreaming, has long been a topic of intense speculation. From the dreams of both August
Kekulé, which led to the conception of a simple structure for benzene (Hubert, 1985), and
Dmitry Mendeleyev, which initiated the creation of the periodic table of elements
(Strathern, 2000), to the late-night dreaming of Otto Loewi, which inspired the
experimental demonstration of neurochemical transmission (Mazzarello, 2000), even
scientific examples of creativity occurring during sleep are not uncommon.
Page 18 of 37

Quantitative data have further demonstrated that solution performance on tests of

cognitive flexibility using anagram word puzzles is more than 30% better following
awakenings from REM sleep compared with NREM awakenings (Walker, Liston, Hobson,
& Stickgold, 2002). Similarly, a study of semantic priming has demonstrated that, in
contrast to the situation in waking, performance following REM sleep awakenings shows
a greater priming effect by weakly related words than by strong primes, while strong
priming exceeds weak priming in NREM sleep (Stickgold, Scott, Rittenhouse, & Hobson,
1999), again indicating the highly associative properties of the REM sleep brain. Even the
study of mental activity (dreams) from REM sleep indicates that there is not a concrete
episodic replay of daytime experiences, but instead a much more associative process of
semantic integration during sleep (Fosse, Fosse, Hobson, & Stickgold, 2003).
Page 19 of 37

Fig. 6.7 Sleep-dependent production of creative Yet, the most striking

insight. (A) Example of the number reduction task. experimental evidence of
Subjects analyze digits in an 8-digit string of 1s, 4s,
sleep-inspired insight is
and 9s, from left to right, using two rules: (i) If two
digits are the same, respond with that digit. Thus,arguably that reported by
starting from the left, the first two digits are both
Wagner and colleagues
“1,” and hence the response (listed below and to the
(Wagner, Gais, Haider,
right of the second digit) is also “1.” (ii) If two digits
are different, respond with the remaining digit. Thus,
Verleger, & Born, 2004).
having produced the response “1,” this response and
Using a mathematical
the next digits are analyzed. Since they differ (“1”
“number reduction
and “4”), the next response is “the remaining digit,
or “9.” This response and the next digit, “4,” also
task” (Thurstone &
differ (“9” and “4”) and so the next response is the
Thurstone, 1941), a
remaining digit, “1.” The analysis is continued to the
end, and the final response, “9” in this case, is the
process of sleep-dependent
solution to the problem. This final response is then
entered as the answer to the problem. However, on creative insight was
elegantly demonstrated.
every trial, the last three response digits (e.g., “4–1–
9” in the figure above) are the mirror image of the
Subjects analyzed and
preceding three (i.e., “9–1–4”). As a result, the
second response digit (circled “9”) always providesworked through a series of
the answer to the problem, resulting in a “shortcut”
8-digit string problems,
to solving the problem, if the subject gains this
hidden insight. (B) Percentage of subjects that using specific addition
gained insight into this hidden rule following an rules (Figure 6.7A).
offline delay while awake across the day, awake
Following initial training,
across the night of following sleep across the night.
after various periods of
*p < 0.05.
wake or sleep, subjects
returned for an additional
series of trails. When retested after a night of sleep, subjects solved the task, using this
“standard” procedure, 16.5% faster. In contrast, subjects who did not sleep prior to
retesting averaged less than a 6% improvement. However, hidden in the construction of
the task was a much simpler way to solve the problem. On every trial, the last three
response digits (e.g., “4-1-9” in Figure 6.7A) were the mirror image (p. 122) of the
preceding three (i.e., “9-1-4”). As a result, the second response digit always provided the
answer to the problem, and using such “insight,” subjects could stop after producing the
second response digit. Most dramatically, nearly 60% of the subjects who slept for a night
between training and retesting discovered this shortcut the following morning (Figure
6.7B). In contrast, no more than 25% of subjects in any of four different control groups
that did not sleep had this insight. Sleeping after exposure to the problem therefore more
than doubled the likelihood of solving it (although it is interesting to note that this insight
was not present immediately following sleep, but took over 100 trials on average to
emerge the next day).
In summary, substantial evidence now suggests that sleep serves a meta-level role in
memory processing that moves far beyond the consolidation and strengthening of
individual memories, and instead aims to intelligently assimilate and generalize these
details offline. In doing so, sleep may offer the ability to test and build common
informational schemas of knowledge, providing increasingly accurate statistic predictions
Page 20 of 37

about the world and allowing for the discovery of novel, even creative next-day solution
insights.
Emotional regulation
Despite substantial research focusing on the interaction between sleep and cognition,
especially memory, the impact of sleep and sleep loss on affective and emotional
regulation has received more limited research attention. This absence of investigation is
perhaps surprising considering that nearly all psychiatric and neurological mood
disorders express co-occurring abnormalities of sleep, suggesting an intimate
relationship between sleep and emotion. Nevertheless, a number of recent studies
evaluating subjective as well as objective measures of mood and affect, combined with
insights from clinical domains, offer an emerging understanding for the critical role of
sleep in regulating emotional brain function.
Affective Reactivity
Together with impairments of attention and alertness, sleep deprivation is commonly
associated with increased subjective reports of irritability and affective volatility (Horne,
1985). Using a sleep restriction paradigm (5 hours/night), Dinges et al. (1997) have
reported a progressive increase in emotional disturbance across a one-week period on the
basis of questionnaire mood scales. In addition, subjective descriptions in participants’
daily journals also indicated increasing complaints of emotional difficulties. Zohar et al.
(Zohar, Tzischinsky, Epstein, & Lavie, 2005) have investigated the effects of sleep
disruption on emotional reactivity to daytime work events in medical residents. Sleep loss
was shown to amplify negative emotional consequences of disruptive daytime events
while blunting the positive benefit associated with rewarding or goal-enhancing activities.
Although these findings help to characterize the behavioral irregularities imposed by

sleep loss, (p. 123) evidence for the role of sleep in regulating our emotional brain is
surprisingly scarce. To date, only one such study has investigated whether a lack of sleep
inappropriately modulates human emotional brain reactivity (Yoo, Gujar, et al., 2007).
Healthy young participants were allowed to sleep normally prior to a functional MRI
scanning session, or were sleep deprived for one night (accumulating approximately 35
hours of total sleep loss). During scanning, subjects performed an affective stimulus
viewing task involving the presentation of picture slides ranging in a gradient from
emotionally neutral to increasingly negative and aversive.
While both groups expressed significant amygdala activation in response to increasingly

negative picture stimuli, those in the sleep-deprivation condition exhibited a remarkable
+60% greater magnitude of amygdala reactivity, relative to the control group (Figures
6.8A & 6.8B). In addition to this increased intensity of activation, there was also a
threefold increase in the extent of amygdala volume recruited in response to the aversive
stimuli in the sleep-deprivation group (Figure 6.8B). Perhaps most interestingly, relative
to the sleep-control group, there was a significant loss of functional connectivity
Page 21 of 37

identified between the amygdala and the medial prefrontal cortex (mPFC) in those who
were sleep deprived—a region known to have strong inhibitory projections and hence
modulatory impact on the amygdala (Sotres-Bayon, Bush, & LeDoux, 2004). In contrast,
significantly greater connectivity in the deprivation group was observed between the
amygdala and the autonomic-activating centers of the locus coeruleus.
Thus, without sleep, an

amplified hyper-limbic
reaction by the human
amygdala was observed in
response to negative
emotional stimuli.
Furthermore, this altered
magnitude of limbic
activity is associated with
a loss of functional
connectivity with the
Click to view larger mPFC in the sleep-
Fig. 6.8 The impact of sleep deprivation on deprivation condition,
emotional brain reactivity and functional implying a failure of top-
connectivity. (A) Amygdala response to increasingly
negative emotional stimuli in the sleep deprivation
down inhibition by the
and sleep control groups, and (B) corresponding prefrontal lobe (Figures
differences in intensity and volumetric extent of 6.8C & 6.8D). It would
amygdala activation between the two groups
(average ± s.e.m. of left and right amygdala). (C) therefore (p. 124) appear
Depiction of associated changes in functional that a night of sleep may
connectivity between the medial prefrontal cortex
(mPFC) and the amygdala. With sleep, the prefrontal
“reset” the correct
lobe was strongly connected to the amygdala, affective brain reactivity to
regulating and exerting and inhibitory top-down next-day emotional
control. (D) Without sleep, however, mPFC
connection was decreased, potentially negating top- challenges by maintaining
down control and resulting in an overactive functional integrity of this
amygdala.
mPFC-amygdala circuit
*p < 0.01; error bars indicate s.e.m.
and thus govern
appropriate behavioral
repertoires (e.g., optimal social judgments and rational decisions). Perhaps most
intriguing, however, is that a similar pattern of anatomical dysfunction has been
implicated in a number of psychiatric mood disorders that express co-occurring sleep
abnormalities (Davidson, 2002; Davidson, Pizzagalli, Nitschke, & Putnam, 2002; New et
al., 2007), directly raising the issue of whether such factors (sleep loss and clinical mood
disorders) are causally related.
Emotional Information Processing

Sleep’s role in declarative memory consolidation, rather than being absolute, may depend
on more intricate aspects of the information being learned, such as novelty, meaning to
extract, and also the affective salience of the material. Independent of the field of sleep
Page 22 of 37

and memory, there is a wealth of evidence demonstrating that memory processing is

modulated by emotion (Cahill, 2000; McGaugh, 2004; Phelps, 2004). Experiences that
evocate emotions are not only encoding more strongly, but appear to persist and even
improve over time as the delay between learning and testing increases (hours/days)
(Kleinsmith & Kaplan, 1963; LaBar & Phelps, 1998; Levonian, 1972; Sharot & Phelps,
2004; Walker & Tarte, 1963).
Although these findings indicate a strong influence of emotion on slow, time-dependent

consolidation processes, based on the coincident neurophysiology that REM sleep
provides and the neurobiological requirements of emotional memory processing (Cahill,
2000; McGaugh, 2004), work has now begun to test a selective REM-dependent
hypothesis of affective human memory consolidation. For example, Hu et al. (Hu, Stylos-
Allen, & Walker, 2006) have compared the consolidation of emotionally arousing and non-
arousing picture stimuli following a 12-hour period across a day or following a night of
sleep. A specific emotional memory benefit was observed only following sleep and not
across an equivalent time awake. Wagner and colleagues (Wagner, Gais, & Born, 2001)
have also shown that sleep selectively favors the retention of previously learned
emotional texts relative to neutral texts, and that this affective memory benefit is present
only following late-night sleep (a time period rich in stage 2 NREM and REM sleep).
Furthermore, this emotional memory enhancement has been shown to persist for several
years (Wagner, Hallschmid, Rasch, & Born, 2006).
Using a nap paradigm, it has most recently been demonstrated that sleep, and specifically
REM neurophysiology, may underlie this consolidation benefit (Nishida et al., unpublished
findings). Subjects performed two study sessions in which they learned emotionally
negative and neutral picture stimuli, one 4 hours prior and one 15 minutes prior to a
recognition memory test. In one group, participants slept (90-minute nap) after the first
study session, while in the other group, participants remained awake. Thus, items from
the first (4-hour) study sessions transitioned through different brain states in each group
prior to testing, containing sleep in the nap group and no sleep in the no-nap group, yet
experienced identical brain-state conditions following the second (15-minute) study
session prior to testing.
No change in memory for emotional (or neutral) stimuli occurred across the offline delay
in the no-nap group. However, a significant and selective offline enhancement of
emotional memory was observed in the nap group, the extent of which was correlated
with the amount of REM sleep and the speed of entry into REM (latency). Most striking,
spectral analysis of the EEG demonstrated that the magnitude of right-dominant
prefrontal theta power during REM (activity in the frequency range of 4.0–7.0 Hz)
exhibited a significant and positive relationship with the amount of emotional memory
improvement.
These findings go beyond simply demonstrating that affective memories are preferentially
enhanced across periods of sleep and indicate that the extent of emotional memory
improvement is associated with specific REM sleep characteristics—both quantity and
Page 23 of 37

quality. Corroborating these correlations, it has previously been hypothesized that REM
sleep represents a brain state particularly amenable to emotional memory consolidation,
based on its unique biology (Hu et al., 2006; Pare, Collins, & Pelletier, 2002).
Neurochemically, levels of limbic and forebrain ACh are markedly elevated during REM
(Vazquez & Baghdoyan, 2001), reportedly quadruple those seen during NREM, and
double those measured in quiet waking (Marrosu et al., 1995). Considering the known
importance of ACh in the long-term consolidation of emotional learning (McGaugh, 2004),
this pro-cholinergic REM state may result in a selective facilitation of affective memories
similar to that reported using experimental manipulations of ACh (Power, 2004). (p. 125)
Neurophysiologically, theta oscillations have been proposed as a carrier frequency
allowing disparate brain regions that initially encode information to selectively interact
offline, in a coupled relationship. By doing so, REM theta may afford the ability to
promote the strengthening of specific memory representations across distributed
networks (Buzsaki, 2002; Jones & Wilson, 2005).
Page 24 of 37

Emotional-Memory Processing: A Sleep To Forget And Sleep To Remember

(SFSR) Hypothesis
Beyond the strengthening of emotional memories, there may be an additional
consequence of sleep-dependent modulation, and one that has significant implications for
mood disorders—that is, sleeping to forget. Based on the emerging interaction between
sleep and emotion, below I outline a model of affective information processing that may
offer brain-based explanatory insights regarding the impact of sleep abnormalities,
particularly REM, for the initiation and/or maintenance of mood disturbance.
While there is abundant evidence to suggest that emotional experiences persist in our
autobiographies over time, an equally remarkable but far less noted change is a reduction
in the affective tone associated with their recall. The reason that affective experiences
appear to be encoded and consolidated more preferentially than neutral memories is due
to autonomic neurochemical reactions elicited at the time of the experience, creating
what we commonly term an “emotional memory.” However, the later recall of these
experiences tends not to be associated with anywhere near the same magnitude of
autonomic (re)activation as that elicited at the moment of learning/experience—
suggesting that, over time, the affective “blanket” previously enveloped around the
memory during encoding has been removed, while the information contained within that
experience (the memory) remains. The hypothesis predicts that this decoupling
preferentially takes place overnight, such that we sleep to forget the emotional tone, yet
sleep to remember the tagged memory of that episode (Figure 6.9). The model further
argues that if this process is not achieved, the magnitude of affective “charge” remaining
within autobiographical memory networks would persist, resulting in the potential
condition of chronic anxiety.
Based on the consistent relationship identified between REM and emotional processing,
combined with its unique neurobiology, this hypothesis proposes that REM sleep provides
an optimal state for achieving such affective “therapy.” Specifically, increased activity
within limbic and paralimbic structures (including the hippocampus and amygdala)
during REM may first offer the ability for reactivation of previously acquired affective
experiences. Second, the neurophysiological signature of REM involving dominant theta
oscillations within subcortical as well as cortical nodes may offer large-scale network
cooperation at night, allowing the integration and, as a consequence, greater
understanding of recently experienced emotional events in the context of pre-existing
neocortically stored semantic memory. Third, these interactions during REM (and
perhaps through the conscious process of dreaming) critically, and perhaps most
importantly, take place within a brain that is devoid of aminergic neurochemical
concentration (Pace-Schott & Hobson, 2002), particularly noradrenergic input from the
locus coeruleus, the influence of which has been linked to states of high stress and
anxiety disorders (Sullivan, Coplan, Kent, & Gorman, 1999). Combined, these
neuroanatomical, neurophysiological, and neurochemical conditions offer a unique
biological theater in which to achieve, on one hand, a balanced potentiation of the
Page 25 of 37

informational core of emotional experiences (the memory), yet may also de-potentiate and
ultimately ameliorate the autonomic charge originally acquired at the time of learning
(Figure 6.9), negating a long-term state of anxiety.
If, however, this process is not achieved across the first night following an emotional
event, the model would predict that a repeat attempt would occur on the second night,
since the strength of emotional “tag” associated with the memory would remain high. If
this process failed a second time, the same events would continue to repeat across
ensuing nights, potentially with an increasing progressive amount of REM in response. It
is just such a cycle of REM-sleep dreaming (nightmares) that represents a diagnostic key
feature of post-traumatic stress disorder. It may not be coincidental, therefore, that these
patients continue to display hyperarousal reactions to associated trauma cues (Harvey,
Jones, & Schmidt, 2003; Pole, 2007), indicating that the process of separating the
affective tone from the emotional experience has not been accomplished. The reason why
such a REM mechanism may fail in post-traumatic stress disorder remains unknown,
although the exceptional magnitude of trauma-induced emotion at the time of learning
maybe so great that the system is incapable of initiating/completing one or both of these
processes, leaving some patients unable to depotentiate, integrate, and hence
“overcome” the experience. (p. 126)
Page 26 of 37

This model also makes

Fig. 6.9 The sleep to forget and sleep to remember
(SFSR) model of emotional memory processing: (A)specific experimental
Neural dynamics of waking formation of an episodic
emotional memory, followed by the subsequent REMpredictions as to the fate
of these two components—
sleep reprocessing, resulting in, on the one hand, a
depotentiation of the affective tone initially
the memory and the
associated with the event(s) at encoding, while on
emotion. As partially
the other, a progressive neocortical consolidation of
the experience in the context of prior semantic demonstrated, the first
knowledge (the conscious expression of which may
prediction would be that,
contribute to dreaming). Cross-connectivity between
over time, the veracity of
structures is represented by number and thickness of
lines. Circles within cortical and hippocampal
the memory itself would
structures represent information nodes; depth of
improve, and the extent to
shade reflects extent of connectivity. Shade fill and
arrows from amygdala represent magnitude of co- which these [negative]
activation and influence on the hippocampus. (B)
emotional experiences are
Conceptual outcome. Through multiple iterations of
this mechanism across the night, and/or across strengthened would be
multiple nights, the long-term consequence of such
proportional to the amount
REM-sleep reprocessing allows for the strengthening
and retention of salient information previously of post-experience REM
tagged as emotional at the time of learning, yet the
sleep obtained, as well as
divorcing of the autonomic charge acquired during
learning. how quickly it is achieved
(REM latency). Secondly,
using autonomic physiology measures, these same predictions would hold in the inverse
direction for the magnitude of emotional reactivity induced at the time of recall. Thirdly, a
pathological increase in REM—as commonly occurs in depression (Armitage, 2007;
Gottesmann & Gottesman, 2007; Tsuno, Besset, & Ritchie, 2005)—may disproportionately
amplify the strength of negative memories, so much so that, despite concomitant
attempts at ameliorating the associated affective tone, would still create a perceived
autobiographical history dominated by negative memory excess (which may also facilitate
disadvantageous waking rumination). (p. 127) In contrast, the selective decrease of REM,
as occurs with many antidepressants, would predict a reduction of such negative memory
consolidation and bias, although may curtail the degree of affect decoupling that can
occur. Long term, the balanced extent of accumulated REM should therefore not only
correlate with the persistence, in memory, of the emotional experience, but it should also
be associated with a decreased magnitude of autonomic response associated with recall—
all of which are testable objectives for future research.
Conclusions
While not fully complete, we will soon have a new taxonomy of sleep-dependent memory
processing, and one that will supersede the polarized all-or-none views of the past
(Stickgold & Walker, 2005; Vertes & Siegel, 2005). With such findings, we can come to a
revised appreciation of how both wake and sleep unite in a symbiotic alliance to
coordinate the encoding, consolidation, and integration of our memories, the ultimate aim
Page 27 of 37

of which maybe to create a generalized yet nonspecific catalog of stored knowledge that
does not rely on the verbose retention of all pervious learned facts.
Beyond memory and plasticity, a growing number of cognitive neuroscience studies, set
on a foundation of clinical insights, point to an exciting role for sleep in regulating
affective brain function and emotional experience. Based on the remarkable neurobiology
of sleep, and REM in particular, a unique capability for the overnight modulation of
affective networks and previously encountered emotional experiences may be possible,
redressing and maintaining the appropriate connectivity and hence next-day reactivity
throughout limbic and associated autonomic systems.
Ultimately, the timeless maternal wisdom of mothers alike may have long held the
answers to Allan Rechtschaffen’s original wisdom; that is, “you should sleep on a
problem,” and when troubled, “get to bed, you’ll feel better in the morning.”
Acknowledgments
The author wishes to thank Edwin Robertson, Robert Stickgold, Allison Harvey, Ninad
Gujar, Els van der Helm, Bryce Mander and Jared Saletin for thoughtful insights.
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Matthew P. Walker
Matthew P. Walker, Department of Psychology & Helen Wills Neuroscience Institute,

University of California, Berkeley.
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The Functions of Sleep

Oxford Handbooks Online

Print Publication Date: Mar 2012 Subject: Psychology, Clinical Psychology

Abstract and Keywords

Keywords: sleep, homeostatic, circadian, environmental factors, memory, emotion

Subscriber: Universiteit Leiden - LUMC; date: 01 November 2018

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The evolution of sleep

The rationale behind an evolutionary approach to understanding sleep processes assumes

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Do all animals sleep?

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Interestingly, when Wehr et al. (1993) looked at extending sleep-time availability in

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An important aspect of Kavanau’s argument (2005, 2006) proposes a separation between

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To Summarize This Position

1. Kavanau (2005, 2006) emphasizes the importance of the relationship between

Current focus on sleep and memory

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Perhaps more remarkably, there is growing evidence to show improvement in

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Vertes (2005) is also critical of sleep-dependent memory process on the strength of

Is all sleep essential?

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Chapter 2 (The Regulation of Human Sleep and Wakefulness)

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Chapter 5 (Sleep and Human Performance)

Chapter 6 (The Role of Sleep in Neurocognitive Function)

Borbély, A. A. (1982). A two-process model of sleep regulation. Human Neurobiology, 1,

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Caldwell, J. A., & Caldwell, J. L. (2005). Fatigue in military aviation: An overview of US

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Durmer, J. S., & Dinges, D. F. (2005). Neurocognitive consequences of sleep deprivation.

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(2008). The effects of modafinil, caffeine and dextroamphetamine on judgments of simple

Kavanau, J. L. (2004). Sleep researchers need to bring Darwin on board: Elucidating

Kavanau, J. L. (2005). Evolutionary approaches to understanding sleep. Sleep Medicine

Kavanau, J. L. (2006). Is sleep’s “supreme mystery” unraveling? An evolutionary analysis

Kavanau, J. L. (2008). Sleepless in the sea. Science, 322, 527.

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McCarthy, M. E., & Williams, W. F. (1997). Decreased attentional responsivity during

Maquet, P. (2000). Functional neuroimaging of normal human sleep by positron emission

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Seligman, M. E. P. (1968). Chronic fear produced by unpredictable shock. Journal of

Shadmehr, R. & Brashers-Krug, T. (1997) Functional stages in the formation of human

Siegel, J. M. (2008). Do all animals sleep? Trends in Neuroscience, 31, 208–213.

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deprivation. Journal of Neuropsychiatry and Clinical Neuroscience, 18, 1–5.

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