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Sleep and the Brain

Article  in  Neuropsychology Review · March 2011

DOI: 10.1007/s11065-011-9156-z · Source: PubMed

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Neuropsychol Rev (2011) 21:1–4
DOI 10.1007/s11065-011-9156-z

REVIEW

Sleep and the Brain

Ian M. Colrain

Received: 4 January 2011 / Accepted: 5 January 2011 / Published online: 25 January 2011
# Springer Science+Business Media, LLC 2011

Abstract Sleep is a fundamental behavior ubiquitous in the measures can be made by asking people to record information
animal kingdom, necessary for the support of physical in a diary. These measures can have high levels of accuracy
health and in humans for the maintenance of cognitive (e.g., lights out time, wake up time) or be more variable (e.g.
function. While it influences all body systems, it is time awake before sleep, time awake during the night)
particularly important for the brain and is typically depending on the individual. Qualitative assessment of sleep
characterized using measures of brain electrical activity. using diaries can also be highly variable based on personality
Sleep undergoes predictable changes across the lifespan, factors and perceived demand characteristics in different
with notably dramatic alterations occurring during adoles- situations. While the effects of sleep are observed in all
cence and with old age. Over and above the normal physiological systems, sleep is typically characterized in the
development changes, however, upwards of a third of the laboratory by measurement of central nervous system activity
adult population experience some form of insomnia on a using electrodes to assess brain activity (electroencephalo-
regular basis. This issue’s special section on “Sleep through graph, EEG), eye movements (electrooculograph, EOG) and
the Ages” contains papers addressing the neurological and muscle activity (electromyograph, EMG). Starting in the
neuropsychological implications of sleep in adolescents, 1930’s (Loomis et al. 1938), sleep researchers have system-
older adults and insomnia sufferers, highlighting relations atically described different states or stages of sleep using
of sleep with brain structure and function. combinations of visually observed EEG, EOG and EMG
signals. A consensus committee published guidelines in 1968
Keywords Polysomnography . Spectral analysis . (Rechtschaffen and Kales 1968) that were used until recently,
Adolescence . Aging . Insomnia when the Academy of Sleep Medicine (Iber et al. 2007)
published what turned out to be only a modest refinement of
Sleep is a complex behavioral state necessary for neurological, the Rechtschaffen and Kales guidelines.
somatic and psychological health throughout the lifespan, Rechtschaffen and Kales (1968) defined two different
affected by the structural and functional condition of the brain, sleep states, Rapid Eye Movement (REM) sleep and non
and influential on neuropsychological performance for better Rapid Eye Movement Sleep (NREM), with NREM sleep
or worse. As is highlighted in the accompanying three papers further subdivided into four stages, labeled 1 through 4, with
by Bastien, Crowley, and Colrain and Baker, measurement of stages 3 & 4 described as being Slow Wave Sleep (SWS).
sleep is challenging. Some quantitative and qualitative The AASM guidelines (Iber et al. 2007) re-labeled stage 1 as
N1, stage 2 as N2, SWS as N3 and REM as R. EEG activity
I. M. Colrain (*)
in both systems is described in terms of the predominant
Human Sleep Research Program, SRI International,
333 Ravenswood Avenue, observed frequency of voltage oscillation, limited by the
Menlo Park, CA 94025, USA band pass filtering of the EEG signal that is typically set at
e-mail: [email protected] between 0.1 and 30 Hz. From slowest to fastest, EEG
activity is described as containing Delta (up to 2 Hz), Theta
I. M. Colrain
Department of Psychological Sciences, University of Melbourne, (4–7 Hz), Alpha (8–12 Hz) and Beta (13–30 Hz) activity.
Parkville, Victoria, Australia Beta is sometimes divided into Beta 1 (13–20 Hz) and Beta
2 Neuropsychol Rev (2011) 21:1–4

2 (>20 Hz) activity. An additional band, Sigma (12–16 Hz), delta frequency waveforms. REM (R) is characterized by
is sometimes described to capture sleep spindles, which are mixed frequency Theta and Beta EEG activity, rapid saccadic
short bursts (0.5–1 s) of synchronized activity within this eye movements in the EOG and a loss of postural muscle tone
frequency range occurring in NREM sleep. in the EMG. The scoring rules applied to these signals allocate
The assumption underlying the mapping of EEG frequency a score to an entire epoch (typically 30, less frequently 20 s)
onto arousal state is based on the extent to which activity based on the activity that is present for at least 50% of that
within the ascending reticular activating system modulates the epoch. Examples of the different stages are presented in
ability of the thalamus to regulate the flow of afferent signals Fig. 1.
to the cortex. High levels of arousal are associated with high The occurrence of sleep stages and states across a night
levels of thalamic throughput resulting in desynchronized is not random, but rather follows an organized pattern
EEG activity sampled by a given electrode, resulting in the termed the “sleep architecture.” Across a normal night’s
appearance if high frequency EEG oscillations. As arousal sleep, there will be four to five sleep cycles, each consisting
level decreases, thalamic throughput decreases and EEG of a period of NREM sleep followed by a period of REM
frequency slows. Sleep-specific synchronized spindle and sleep, and each lasting around 90 min. The NREM periods
Delta activity are seen when the thalamocortical network have more SWS in the beginning of the night (cycles 1 and
experiences burst firing due to hyperpolarization of thalamic- 2) and more stage 2 later in the night, whereas the REM
relay neurons (Steriade 1997). periods tend to be longer in the later cycles, thus most SWS
Wake is thus characterized as having desynchronized occurs early in the night and most REM sleep later.
mixed frequency Beta activity and a synchronized single Although this basic architecture stays remarkably stable
frequency Alpha activity. Stage 1 (N1) is characterized by the across the lifespan, marked developmental changes occur in
significant intrusion of Theta activity into an EEG epoch and some features of sleep. For example, SWS shows high
is often associated with slow rolling eye movements in the levels in childhood that rapidly decline with adolescence
EOG. Stage 2 (N2) is characterized by the presence of mixed and then gradually continue to decline to very low levels in
frequency theta activity, K-complexes (single, large Delta old age (Fig. 2, issue cover). Interruptions in sleep by
frequency waveforms) and/or sleep spindles. SWS (N3) is periods of wakefulness, rare in children, also increase with
characterized by a significant inclusion of large (>75 μV) age and can be a prominent feature of sleep in the elderly.

Fig. 1 Examples of sleep stages

from the one healthy 21 year-old
man. In each case 30 s of data are
presented for electrodes Fz, Cz
and O2 together with a single
channel of EOG data from elec-
trodes placed superior to the left
outer canthus and inferior to the
right outer canthus, and a single
channel of submentalis EMG. A:
alpha activity (continuous in O2
while awake, brief burst at Cz in
stage 1). B: Theta activity; C:
Rolling eye movements; D: K-
complex; E: sleep spindle; F:
delta activity; Rapid eye
movements
Neuropsychol Rev (2011) 21:1–4 3

Fig. 2 Examples of sleep archi-

tecture hypnograms, SWS EEG,
and brain structure in women of 14 year old
from adolescence to older age.
Left column: The top of each panel
displays a hypnogram, reflecting
the distribution of sleep stages
across the night. Wakefulness is
represented as blank space, stage 1
in yellow, stage 2 in green, stage 3
in light blue, stage 4 in dark blue
and REM sleep in red. Under each
hypnogram are EEG tracings from
three frontal sites (F3, Fz, and F4),
three central sites (C3, Cz, and
C4), and two occipital sites (O1
and O2), all referenced to a con-
tralateral earlobe electrode (A1 or
A2). The scaling in all panels is 32 year old
identical at 500 μV per channel.
The 14 year-old girl was in SWS
(stage 3 + stage 4) for 33% of the
night, the 32 year-old woman was
in SWS for 13% of the night, and
the 62 year-old woman for 4% of
the night. Right column: The brain
images are parasagittal views tak-
en from 3T anatomical proton
density weighted (SPGR) mag-
netic resonance images (MRIs) of
a 14 year old girl, a 32 year old
woman, and a 62 year old women,
each in good health. The MRI
studies are courtesy of Adolf
Pfefferbaum, M.D., Director of the 62 year old
Neuroscience Program, SRI Inter-
national, Menlo Park, CA and
Professor Emeritus, Stanford Uni-
versity School of Medicine

Since the 1940’s (Brazier 1949), attempts have been made neuropsychological function during wakefulness in adoles-
to characterize sleep EEG in a more continuous way than by cence, adulthood and old age. They also highlight how
staging using power spectral analysis (PSA) (Fig. 3). changes in sleep across the lifespan can be viewed as a
Although not used for clinical judgments of sleep, PSA reflection of changes in brain structure, brain function or both.
techniques are often used in research to evaluate develop- They address three populations representing ontological
mental changes in EEG or to show the intrusion of wake-like development. Adolescence is a period of dramatic changes
EEG (Alpha and Beta frequencies) into sleep or drowsy EEG in physical, neurological and psychological function often
(Theta activity) into wakefulness. Beta power during sleep is accompanied by dramatic increases in risk taking behavior
a common measure of arousal during sleep in insomnia (Eaton et al. 2010). Insufficient sleep during this period can
(Perlis et al. 2001). Delta power, often termed slow wave exacerbate risks and lead to poor educational and health
activity (SWA), is commonly used as a marker of sleep outcomes (Dewald et al. 2010). Adult insomnia is the most
pressure and is homeostatically regulated (Feinberg 1974). prevalent sleep problem in society with nearly a third of the
The three papers in this section highlight how changes in population experiencing some form of sleep difficulty on a
sleep correlate with a number of aspects of behavior and regular basis. Total estimated costs to society of health care,
4 Neuropsychol Rev (2011) 21:1–4

Fig. 3 Adapted from

Buckelmuller et al. (2006)
showing the all-night EEG
power spectra in non-REM sleep
in baseline nights 1–4 of
subject a single subject (a) and
in 8 different subjects (b). The
data highlight the dominance of
the slow frequency activity and
the peak at around 14 Hz
corresponding to sleep spindles.
While there is individual varia-
tion, the pattern of power distri-
bution is highly consistent
within subjects from night to
night

self medication and lost productivity are in the tens of Buckelmuller, J., Landolt, H. P., Stassen, H. H., & Achermann, P.
billions of dollars annually in the U.S. alone (Siebern and (2006). Trait-like individual differences in the human sleep
electroencephalogram. Neuroscience, 138(1), 351–356.
Manber 2010). The aging of the post World War II “baby
Dewald, J. F., Meijer, A. M., Oort, F. J., Kerkhof, G. A., & Bogels, S.
boom” population is already providing an increased load on M. (2010). The influence of sleep quality, sleep duration and
health care systems. Changes in sleep with normal aging can sleepiness on school performance in children and adolescents: a
exacerbate other health issues, and adequate management of meta-analytic review. Sleep Medicine Reviews, 14(3), 179–189.
Eaton, D. K., McKnight-Eily, L. R., Lowry, R., Perry, G. S.,
sleep in the elderly population has the potential to reduce
Presley-Cantrell, L., & Croft, J. B. (2010). Prevalence of
total health care burden. insufficient, borderline, and optimal hours of sleep among high
Despite the lack of a grand unifying theory of sleep school students—United States, 2007. The Journal of Adolescent
specifying a single function, the consequences of poor or Health, 46(4), 399–401.
Feinberg, I. (1974). Changes in sleep cycle patterns with age. Journal
inadequate sleep and elevated daytime sleepiness are
of Psychiatric Research, 10(3–4), 283–306.
clearly detrimental to physical, neurological, neuropsycho- Iber, C., Ancoli-Israel, S., Chesson, A., & Quan, S. F. (2007). The AASM
logical and psychological health. The purpose of this manual for the scoring of sleep and associated events: Rules,
special section of the journal on sleep, is to provide a terminology and technical specifications (1st ed.). Westchester:
American Academy of Sleep Medicine.
thoughtful and empirically-based exposition of what should
Loomis, A., Harvey, E., & Hobart, G. (1938). Distribution of disturbance-
be expected in terms of sleep duration and quality at patterns in the human electroencephalogram, with special reference
different points in the post-childhood lifespan and to to sleep. Journal of Neurophysiology, 1, 413–430.
document the pressures placed on sleep by medical and Perlis, M. L., Kehr, E. L., Smith, M. T., Andrews, P. J., Orff, H., &
Giles, D. E. (2001). Temporal and stagewise distribution of high
psychological problems, physiological changes and societal
frequency EEG activity in patients with primary and secondary
pressures and how all of these factors can affect measurement insomnia and in good sleeper controls. Journal of Sleep
of neuropsychological performance. Research, 10(2), 93–104.
Rechtschaffen, A., & Kales, A. (1968). A manual of standardised
terminology, techniques and scoring systems for sleep stages of
human subjects. Washington D.C.: U.S. Government Printing Office.
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