Sleep, \6:S65-S67
© 1993 American Sleep Disorders Association and Sleep Research Society
(b) ViligancelSleepiness Sequelae of
Sleep Disordered Breathing and Sleep Apnea
Cognitive Effects of Sleep and Sleep Fragmentation
M. H. Bonnet
Dayton Veterans Administration Medical Center, Wright State University, and
Kettering Medical Center, Dayton, Ohio, US.A,
Patients with sleep apnea frequently report changes
in cognitive function, including poor memory, confusion, irritability and sleepiness. One means of determining which of these symptoms are secondary to
the sleep disturbance caused by the sleep apnea as compared to the oxygen desaturation and other physiological effects of apnea is to study the effects of sleep and
sleep disturbance alone on various cognitive abilities.
This paper summarizes two experiments that have examined sleep, sleep disturbance and cognitive ability
in normal young adult subjects.
Obviously, being asleep greatly reduces cognitive
ability. When one is awakened from sleep, ability to
perform a broad range of tasks is also reduced for a
period of time ranging from a few seconds to 30 minutes (1). This poor performance related to the process
of arousal has been called "sleep inertia". Sleep inertia
effects were illustrated in a study of memory after
awakening from sleep (2). Fourteen subjects slept in
the laboratory for five nights. After adaptation, subjects had one of four randomized memory conditions
on each night. On one night, subjects were awakened
out of stage 2 (light) sleep and performed the Williams
word memory task immediately upon awakening. On
another night, subjects were awakened out of stage 4
(deep) sleep and performed the Williams word memory
task immediately upon awakening. On another night,
subjects were awakened out of stage 4 (deep) sleep and
performed the Williams word memory task followed
by a maze-tracing task. On another night, subjects were
awakened out of stage 4 (deep) sleep and performed
the maze tracing task followed by the Williams word
memory (WM) task. In all conditions, subjects were
allowed to return to sleep following testing and had a
final recall test for the words presented on the preceding
evening when they awoke in the morning.
The results of this study are presented in Fig. 1,
which presents long-term recall data (which had results
identical to the short-term recall data). It can be seen
from the figure that recall was decreased significantly
when subjects had been awakened from deep sleep
(stage 4) as compared to light sleep (stage 2). It can
also be seen that recall was significantly decreased when
subjects performed the memory task immediately after
awakening as compared to performing the memory
task after they had been awake for eight minutes (WM2
versus WMl). This data indicates that memory ability
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FIG. 1. Mean number of words recalled in the long-term memory
task. ST2 is the stage 2 awakening; ST4 is the stage 4 awakening;
WM 1 is the stage 4 awakening immediately followed by the memory
task; WM2 is the stage 4 awakening with the memory task 8 minutes
after awakening,
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M. H. BONNET
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Response Latencies At Six Times Across Nights 1 and 2
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FIG. 2. Latency to give a verbal response to a two-digit two-number addition problem given after arousal from sleep in three different
arousal conditions across two nights of experimental sleep disturbance.
after awakening from sleep decreases as a function of
how deeply the subject was sleeping before awakening.
Memory ability is also increased as a function of how
long the subject was awake before the memory task.
In this study, memory ability immediately after awakening from stage 2 sleep was about the same as memory
ability 8 minutes after awakening from stage 4 sleep.
A patient with sleep apnea has frequent arousals
during sleep as he attempts to resume respiration. In
a series of studies, we have shown that when normal
young adults have their sleep disturbed in a manner
similar to the disturbance seen in patients with severe
sleep apnea, the normal young adults begin to demonstrate symptoms of sleep deprivation. Specifically,
when young adults have their sleep significantly fragmented, they become increasingly sleepy during the
day and at night; they begin to sleep more deeply (i.e.
have higher arousal thresholds during sleep); their ability to perform psychomotor tasks, such as vigilance,
Sleep. Vol. 16, No.8, 1993
addition, and reaction time decreases (3) and they
demonstrate rebound slow wave sleep and rapid eye
movement (REM) sleep when allowed to sleep without
disturbance.
One study has looked specifically at depth of sleep
and cognitive ability in young adults as their sleep has
been fragmented on three different schedules (4). In
this study, a group of young adult subjects had two
consecutive nights of experimental sleep disturbance
repeated at three different times. In one two-night period, subjects were briefly awakened after each minute
of electroencephalograph (EEG) defined sleep. In a second two-night period, subjects were briefly awakened
after each 10 minutes of EEG defined sleep. In a final
two-night period, subjects were allowed to sleep for 2.5
hours and were then briefly awakened at sleep onset
for the remainder of the night. Each awakening was
performed with an audiometer so that standard auditory arousal thresholds could be determined. After
SLEEP FRAGMENTATION AND MEMORY
alternate awakenings, subjects were asked to solve
mentally and report verbally solutions to a random
two-digit and two-number addition problem. Latency
in seconds from the presentation of the problem to the
response was recorded. Latencies to correct and incorrect responses did not differ and were therefore
combined. Average response latencies as a function of
time of night, night of disturbance and experimental
condition were plotted in Fig. 2.
A significant condition by night interaction (F2.32 =
1l.9, p < 0.01) was found. Post-hoc comparisons
(Newman-Keuls at p < 0.05) showed that latencies
were longest after the 10-minute condition on the first
night. However, on the second night, latencies were
longest in the I-minute condition. This interaction suggests that the sleep inertia or nocturnal confusion effects built up more rapidly when sleep was frequently
interrupted. Response difficulty increased most slowly
when subjects were allowed a 2.5-hour period of consolidated sleep. Subjects took 7 seconds to solve these
problems under non sleep control conditions. The magnitude of increase in response latency, from about 15
seconds to almost 1 minute after frequent arousals,
suggests major changes in ability to process information and make responses. In fact, it became very difficult to arouse some subjects at all despite the use of
l20-dB tone intensities. Other subjects would give
nonsensical or even non-English responses. Some subjects reported in the morning that they had heard the
technician talking to them but could not remember
how to speak to respond. Subjects usually estimated
that they had been awakened 12-14 times per night
when they had actually been awakened on the average
120 times per night in the I-minute awakening condition. Finally, a significant but relatively low level
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correlation (r = 0.32, p < 0.05) was found between
response latency and arousal threshold.
In summary, these data suggest that the sleep disturbance commonly found in patients with sleep apnea
can result in profound changes in cognitive ability during the night. These changes, which include poor longterm memory for events occurring during the night,
are consistent with cognitive processing changes that
occur following sleep deprivation (3) and which may
be related to increasing depth of sleep. More extreme
events such as nocturnal confusion may also be a direct
effect of sleep loss. The reported decrements occurred
very rapidly. Furthermore, patients with severe sleep
apnea usually have additional sleep periods during the
day. As a result of increasing sleep depth and sleep
inertia, it is therefore likely that sleep inertia will cause
sleep-related deficits in both short-term and long-term
memory throughout the day in these patients.
Acknowledgement: This work was performed at the Lorna
Linda Veterans Administration Medical Center and supported by a Merit Review Grant from the Department of
Veterans Affairs.
REFERENCES
I. Dinges DF. Napping patterns and effects in human adults. In:
Dinges DF, Broughton RJ, eds. Sleep and alertness chronobiological. behavioral. and medical aspects of napping. New York:
Raven Press, 1989: 171-204.
2. Bonnet MH. Memory for events occurring during arousal from
sleep. Psychophysiology 1983;20:81-7.
3. Bonnet MH. Sleep deprivation. In: Kryger M, Roth T, Dement
we, eds. Principles and practice of sleep medicine. 2nd ed. New
York: Saunders, 1993 (in press).
4. Downey R, Bonnet MH. Performance during frequent sleep disruption. Sleep 1987; I 0:354-63.
Sleep. Vo!' 16, No.8, 1993