Sleep Research Online 5(3): 89-97, 2003
http://www.sro.org/2003/Cavallero/89/
Printed in the USA. All rights reserved.
1096-214X
© 2003 WebSciences
Stage at Awakening,
Sleep Inertia and Performance
Corrado Cavallero and Francesco Versace
Department of Psychology, University of Trieste, Italy
Our purpose was to verify if the differential effect of final stage at awakening varies with the amount of sleep reduction and
if this effect goes beyond the boundaries of sleep inertia. Seven university students were paid for their participation. The
design included two conditions, REM (three consecutive nights) and NREM (three consecutive nights). Sleep length was
progressively curtailed to 6 hrs, 4.5 hrs and 3 hrs for the first, second and third night, respectively. In the REM condition,
participants were awakened during REM sleep, while in the NREM condition, participants were awakened during Stage 2.
Days following experimental nights were devoted to the assessment of performance. Test sessions were scheduled upon
awakening and then every three hours thereafter. Performance was measured by means of a Simple Reaction Time task and
a Four Choice reaction time task. Results show that sleep inertia after NREM awakenings is more pronounced than after REM
awakenings. Sleep curtailment enhances this differential effect and prolongs it beyond sleep inertia boundaries. Final stage
at awakening not only exerts a differential influence on performance within the sleep inertia phase, but also impairs
performance after NREM awakenings following inertia dissipation, especially when sleep is curtailed.
CURRENT CLAIM: Sleep inertia following Stage 2 awakenings is more pronounced than after REM awakenings; sleep
curtailment enhances this differential effect and prolongs it beyond sleep inertia boundaries.
When waking from sleep, people usually experience a period
of confusion in which performance, compared to pre-sleep
levels, is impaired. This phenomenon, which is most dramatic
and evident when awakening is abrupt, is known as “sleep
inertia” and has been observed by a great number of researchers
(Kleitman, 1963; Lubin et al., 1976; Naitoh, 1981; Dinges et al.,
1981, 1985, 1987; Bonnet, 1983, 1993; Balkin and Badia, 1988;
Dinges, 1989, 1990; Pivik, 1991; Naitoh et al., 1993; Mullington
and Broughton, 1994; Bonnet and Arand, 1995).
Sleep inertia reflects the graduality of the awakening
process, just as increasing sleepiness characterizes the
transitional state of sleep onset. The question of whether sleep
inertia and sleepiness are of the same nature is still debated.
Balking and Badia (1988) failed to find any conclusive
evidence suggesting that sleep inertia is qualitatively different
from typical sleepiness. Tassi and Muzet (2000), in their recent
review of the literature, hypothesize that performance
decrements observed in sleep inertia are due to lowered levels
of arousal, while sleepiness is a state of hypo-vigilance and
furthermore, that both states share the slowing down of
reaction times but only sleepiness involves a reduction in
performance accuracy.
Regardless of its nature, sleep inertia is typically modest
and short-lived following awakening from a night with a
normal amount of sleep (Dinges, 1990). Sleep
deprivation/reduction tends to increase its intensity (Dinges et
al., 1985; Balkin and Badia, 1988) and duration (Naitoh, 1981;
Dinges et al., 1987), even if results on duration have been
inconsistent. For example, Naitoh (1981) found that after 50
hrs of sleep deprivation, sleep inertia lasted for several hours,
while Dinges et al. (1987) showed that, even after 56 hrs of
sleep deprivation, sleep inertia never lasted more than 30
minutes. This discrepancy, as pointed out by Muzet et al.
(1995), is probably attributable to differences in the
experimental designs and tasks used in the various studies.
However, even if duration estimates vary from 1 minute (Webb
and Agnew, 1964) to several hours (Naitoh, 1981), the various
authors tend to agree on a maximum of 3-4 hrs.
Sleep stage at awakening is an important factor in
amplifying sleep inertia: waking up from slow wave sleep
(SWS) is worse than waking up from REM sleep (Dinges et
al., 1985). Less is known about the relationship between other
NREM stages and performance, even if Scott (1969) made an
attempt at studying performance as a function of the sleep
stage from which participants are aroused. The author states,
“Preliminary results ... indicate ... progressively greater
impairment in relation to Stage 1-REM, 2 and 3+4,
respectively.”
Thirty years later, Jewett et al. (1999) analyzed the time
course of inertia dissipation following REM and Stage 2
awakenings in participants who slept an average of 8 hrs per
night and found that sleep inertia effects dissipate in about 3
hrs in both conditions but failed to find any final sleep stage
effect on performance. This failure could be due to the amount
of sleep preceding the final awakening; indeed, if curtailing
sleep time enhances sleep inertia, it is reasonable to presume
that partially depriving participants of sleep can also amplify
the differential effect of sleep stage at awakening on sleep
inertia. However, this line of reasoning can only be followed at
a hypothetical level, as we were not able to find a single study
that specifically investigated final stage effects in partially
sleep-deprived participants.
Correspondence: Corrado Cavallero, Ph.D., University of Trieste, Department of Psychology, Via S. Anastasio 12, 34134 Trieste, Italy,
Tel: 39-040-5582729, Fax: 39-040-4528022, E-mail: [email protected].
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CAVALLERO AND VERSACE
Another much debated question refers to the duration of
both sleep inertia and differential final stage effects. On the one
hand, there is no general agreement on how long sleep inertia
lasts: duration estimates vary from 1 minute (Webb and
Agnew, 1964) to several hours (Naitoh, 1981), even if the
various authors seem to agree on a maximum duration of 3-4
hrs. On the other hand, the only study that investigated the time
course of sleep inertia following awakening from REM and
NREM sleep (Jewett et al., 1999) failed to find a differential
effect, even upon awakening.
Moreover, nearly nothing is known about what happens
beyond the agreed end point of the time course of sleep inertia.
In particular, does sleep stage at awakening exert any
differential effect on performance during the period that goes
from hypothesized sleep inertia dissipation to successive sleep
onset?
In order to answer some of these questions, one has to
devise an experimental design which allows for a) the
comparison of the same participant’s performance following
awakenings alternatively in REM and NREM conditions; b)
the shortening of a comparable amount of sleep granted to each
participant; and c) the keeping constant of–together with the
amount of sleep granted to each participant–the circadian
phase in which participants are awakened. Keeping these
premises in mind, the only viable solution seems to be
comparison between awakenings in REM and Stage 2. In fact,
a comparison between REM and SWS awakenings, a situation
in which the most pronounced effects, if any, would be
expected, would not allow for simultaneous control of sleep
amount and circadian phase.
The present study, which was designed following the above
mentioned criteria, allows us to compare performance
following awakenings in REM and NREM-Stage 2 in two
different sleep reduction conditions (Low and High) in order to
verify a) if the differential effect of final stage at awakening
varies according to the amount of sleep reduction; and b) if this
effect goes beyond what is commonly defined as the boundary
of sleep inertia effects.
In particular we proposed three main hypotheses: A) The
average daily level of performance is better following awakening
in REM than in NREM-Stage 2; B) The difference between REM
and NREM awakenings in the average daily level of performance
increases (or becomes significant) in the High Sleep Reduction
Condition; C) In the High Sleep Reduction Condition, the
difference in performance following REM and Stage 2 awakenings
persists during the period that goes from hypothesized sleep inertia
dissipation to successive sleep onset.
types. Participants were told that they would be submitted to a
reduced sleep schedule and their performance would be tested
during the day, at fixed intervals. They were asked to maintain their
habitual physical activity and study routines, to reduce caffeine
consumption, and to not sleep during the experimental days.
Experimental Design
The entire experimental period was divided into three
different conditions: Adaptation (one night), REM (three
consecutive nights), and NREM (three consecutive nights).
These took place in three different weeks according to the
following schedule: Adaptation (1st week), REM and NREM
in the following two weeks in counterbalanced order.
During the Adaptation night, each participant slept
following his/her own habitual sleep schedule in order to
facilitate adaptation to the lab situation and determine sleep
duration and architecture.
In the REM condition, each participant underwent
progressive sleep reduction and was awakened during the
fourth REM phase (1st day–REM Baseline), during the third
REM phase (2nd day–Low Sleep Reduction), and during the
second REM phase (3rd day–High Sleep Reduction).
Participants were awakened ten minutes after the appearance
of the first clear REM burst. In the NREM condition,
participants were always awakened in Stage 2, in the effort to
obtain comparable amounts of sleep reduction1. In both REM
and NREM conditions, participants were allowed to sleep for
about six hours (roughly corresponding to four sleep cycles)
during the first night (Baseline), for about four and a half hours
(three sleep cycles) the second night (Low Sleep Reduction),
and for about three hours (two sleep cycles) the third night
(High Sleep Reduction) (Figure 1).
During the wake period following each night, performance
levels were assessed in test sessions that took place at fixed
intervals. The first test session started immediately after
awakening and then every three hours according the following
schedule: 8 a.m., 11 a.m., 2 p.m., 5 p.m., 8 p.m., and 11 p.m.,
with the exception of Day 3 in both REM and NREM
Figure 1
Experimental
Design
Experimental Design
Baseline
A
R
E
M
1
11
14
17
20
23
Low Sleep Reduction
A
8
11
14
17
20
23
High Sleep Reduction
5
A
8
11
14
17
20
23
8
11
14
17
20
23
Low Sleep Reduction
A
8
11
14
17
20
23
High Sleep Reduction
5
A
8
11
14
17
20
23
Baseline
METHODS
Participants
Eight normal sleepers (four males and four females, aged 20
to 26), all university students, were studied in pairs in the sleep
laboratory. On the basis of the results of the
Morningness/Eveningness Questionnaire (MEQ, Horne and
Ostberg, 1976), all participants were classified as intermediate
8
N
R
E
M
A
A Awakening
NREM Sleep
Wake
REM Sleep
Testing
When the NREM condition was run before the REM condition, the awakening time was determined with reference to the sleep architecture of the adaptation night.
91
STAGE AT AWAKENING, SLEEP INERTIA AND PERFORMANCE
conditions, where an additional 5 a.m. test session took place
(Figure 1). During the time intervals between test sessions,
participants were allowed to perform activities of their choice
(work, study, etc.) but were not allowed to sleep.
In order to avoid the masking effects of a learning curve,
all participants had a practice session before the beginning of
the adaptation night and before the beginning of the first
experimental night in each condition.
Procedure
Adaptation
At 9 p.m., participants arrived at the lab where they
received instructions regarding the following day’s schedule
and then practiced with the test battery for about one and a half
hours, performing each task 10 times. At 11 p.m. (mean time),
participants were prepared for the night. Two unipolar EEG
(F3-A1, F4-A1) and two EOG (LE-A2, RE-A2) channels were
recorded during the night. At 12:40 a.m. (mean time)
participants went to bed and lights were turned off. Sleep onset
was assessed by the appearance of the first clearly identifiable
K-complex and/or sleep spindle.
The following morning, one hour after being awakened,
participants underwent another practice session (10 rounds of
each performance task) and then they left the sleep laboratory.
Experimental Conditions
At 10 p.m., participants arrived at the laboratory. They
practiced with the test battery for a while (completing three
sessions of each performance task) and were then prepared for
the night following the above-mentioned procedure. At 12:20
a.m. (mean time), participants went to bed and lights were
turned off. After being awakened, participants were tested
following the same schedule for both experimental conditions,
as illustrated in Figure 1.
Materials
Each test session lasted about 10 minutes and consisted of
three parts: a) measurement of timpanic temperature (by means
of a Thermoscan Plus thermometer, Thermoscan Inc.); b)
assessment of subjective vigilance levels (Stanford Sleepiness
Scale (SSS) [Hoddes et al., 1973], and Global Vigor/Affect Scale
(GVAS) [Monk, 1989]); and c) assessment of performance
levels by means of two tests (described below) presented in
randomized order.
The seven statements of the SSS appeared on the computer
screen, and the participant made his/her choice by pressing the
corresponding key on the numerical keyboard of the computer.
The GVAS was administered in a paper and pencil version.
The two performance tests had been previously created with
the Micro Experimental Laboratory (MEL) software (Schneider,
1988, 1990), and they ran on 486 IBM compatible computers.
The first was a Simple Reaction Time Task (SRTT). In this
test, participants are asked to press the keyboard space bar
immediately after the presentation of a red circle on the
computer screen, presented 60 times at randomized intervals
2
(Inter-Trial Interval (ITI) ranging from 600 to 2000 msecs). The
entire task takes about two minutes.
The second was a Four-Choice Reaction Time Task
(4CRTT). In this test, the target (a red circle) is presented in
one of four different positions arranged in a square on the
computer screen. Participants are asked to press the key on the
numeric keypad corresponding to the position of the target as
fast as possible. The total number of trials is 40, ten for each
possible target position, presented with a 1000 msecs ITI for a
total duration of about two minutes.
The dependent variables were reaction times for the SRTT
and reaction times plus error rates for the 4CRTT.
RESULTS
Physiological Data
Sleep recordings were independently scored according to
Rechtschaffen and Kales’s criteria by two experienced scorers
(the two authors), who reached an interscorer reliability of 0.89.
Discrepancies were then reconciled and all analyses were
performed on the reconciled version. No discrepancies were
found regarding sleep stage at awakening. As a result of this
analysis, one participant had to be excluded from the original
sample, because her awakenings did not conform to standards2.
Further analyses were therefore carried out on the data from the
remaining seven participants (four who had followed the REMNREM schedule and three the NREM-REM schedule).
To verify the comparability of the intensity of sleep
reduction in the REM and NREM conditions, total sleep time
(TST) was used as dependent variable in a two-way (Condition
by Day) ANOVA. Not surprisingly, we found a significant main
effect for Day (F2,12=186.20; p<0.0001; average TST for Day 1
(Baseline) was 335.83±10.50 minutes, Day 2 (Low Sleep
Reduction) was 271.33±17.62, Day 3 (High Sleep Reduction)
was 183.83±12.21 minutes), while the interaction Condition by
Day was not significant (Table 1). Since the above analysis
showed that the two conditions were comparable regarding TST
for the three sleep reduction levels, we proceeded analyzing
sleep architecture for the two conditions within each day. Three
ANOVAs were performed (one for each day) using Condition
(REM and NREM) and Sleep Stage (Stage 1, Stage 2, SWS,
REM, Movement and Wake Time after Sleep Onset) as factors.
The interaction Condition by Stage was not significant in any of
the three ANOVAs, thus indicating no main differences in sleep
architecture between the REM and NREM conditions. Mean
percentages of each sleep stage for the three days in REM and
NREM are shown in Table 1.
As far as sleep efficiency (time asleep/time in bed) is
concerned, we found no difference between the two conditions
or among the three days (Table 1).
Temperature data for both REM and NREM Conditions were
subjected separately to Cosinor Analysis to verify if
experimental condition affected circadian rhythmicity. Table 2
presents the results derived from the analyses, where it can be
noted that circadian rhythmicity is maintained in both
conditions with no major differences between the two.
One awakening, initially classified as NREM, was indeed a REM one; thus, the NREM condition was incomplete.
92
CAVALLERO AND VERSACE
Table 1
Sleep Measures for Baseline, Low and High Sleep Reduction
in REM and NREM Conditions
SR
AC
REM
Baseline
NREM
Low Sleep Reduction
REM
NREM
High Sleep Reduction
REM
NREM
TST
Mins
344.82
(16.76)
326.84
(18.71)
273.12
(31.98)
269.55
(6.38)
184.13
(14.41)
183.53
(14.41)
St1
%
1.39
(1.14)
1.27
(0.72)
0.92
(0.87)
1.23
(0.71)
1.86
(0.88)
1.28
(1.04)
St2
%
46.99
(4.89)
50.23
(3.25)
45.60
(8.62)
42.10
(4.42)
26.21
(8.50)
31.06
(4.83)
SWS
%
27.40
(8.40)
25.46
(4.33)
34.29
(3.67)
35.40
(8.70)
54.93
(12.30)
51.65
(8.40)
REM
%
18.62
(5.97)
17.67
(5.62)
14.63
(5.67)
15.41
(6.83)
12.09
(4.58)
10.90
(6.62)
W
%
1.22
(2.50)
0.95
(1.47)
0.41
(0.49)
0.22
(0.23)
0.21
(0.23)
0.58
(0.85)
M
%
4.38
(0.55)
4.42
(2.16)
4.15
(1.57)
5.64
(5.64)
4.70
(1.89)
4.53
(2.83)
SE
%
91.11
(2.76)
88.46
(5.88)
90.30
(5.94)
91.22
(7.71)
89.37
(2.92)
91.00
(3.61)
NOTE: SR=Sleep Reduction; AC=Awakening Condition; TST=Total Sleep Time; St1=Stage 1; St2=Stage 2; SWS=Slow Wave Sleep;
REM=Rapid Eye Movement Sleep; W=Wake Time; M=Movement Time; SE=Sleep Efficiency.
Table 2
Cosinor Summary of Temperature Circadian Rhythm in REM and NREM Conditions
Condition
N
PR
Mesor(SD)
Amplitude
Mean (95% CI)
Acrophrase (h min)
Mean (95% CI)
REM
7
45.32
36.40 (0.32)
0.29 (0.17 to 0.42)
16.06 (14.21 to 17.50)
NREM
7
38.65
36.27 (0.28)
0.27 (0.12 to 0.42)
17.01 (15.09 to 18.53)
NOTE: PR=Percent Rhythm–measure of the strength of the circadian rhythm; Mesor=Rhythm-determined average; Amplitude=measure of
one-half the extent of rhythmic change in a cycle; Acrophase=peak time with reference to local midnight.
Subjective Data
For each condition (REM and NREM) and for each
scale–SSS and GVA (separately for Vigor and Affect
subscales)–mean values were calculated for test sessions
between the hours of 11 a.m. and 11 p.m. in the Baseline
condition. All values from the Low and High Sleep Reduction
conditions were then converted into deviations from these means
in order to eliminate the effects of interindividual differences.
Mean deviation scores were then calculated for four different
periods: Awakening; Morning (averaging the 8 a.m. and 11 a.m.
sessions for Low Sleep Reduction and the 5 a.m., 8 a.m., and 11
a.m. sessions for the High Sleep Reduction conditions);
Afternoon (averaging the 2 p.m. and 5 p.m. sessions); and
Evening (averaging the 8 p.m. and 11 p.m. sessions).
Deviation scores for each scale (SSS and GVA–separately for
the Vigor and Affect subscales) were used as dependent
variables in a three-way ANOVA with Awakening Condition
(REM and NREM), Sleep Reduction (Low and High) and Period
(Awakening, Morning, Afternoon, and Evening) as factors.
Stanford Sleepiness Scale. We found significant main
effects of a) Sleep Reduction (Low=0.83±0.41; High=1.59±0.41;
F1,6=46.59; p=0.0005); b) Period (Awakening=2.39±0.87,
Morning=0.83±0.34,Afternoon=0.62±0.40, Evening=1.00±0.46;
F3,18=20.01; p<0.0001). Post-hoc comparisons for Period showed
that the mean deviation at Awakening was significantly different
from those at Morning, Afternoon and Evening (Tukey’s HSD,
p<0.05), while no significant differences among these last three
periods could be detected. No interaction reached significance.
Global Vigor Affect. Regarding the VIGOR subscale,
we found significant main effects of a) Sleep Reduction
(Low= -11.71; High = -20.89; F1,5=12.48; p=0.0167); b) Period
(Awakening= -30.92, Morning= -12.97, Afternoon= -8.84,
Evening= -12.45; F3,15=6.48; p=0.005). Post-hoc comparisons for
Period showed that the mean deviation at Awakening is
significantly different from those at Morning, Afternoon and
Evening (Tukey’s HSD, p<0.05), while no significant differences
among these last three periods could be detected. Again, no
interaction reached significance.
As far as the AFFECT subscale is concerned, no significant
differences were found for main or interaction effects.
Performance Data
Reaction Time
For each condition (REM and NREM) and for each task
(simple and four-choice reaction time), mean reaction times
were calculated for test sessions between the hours of 11 a.m.
and 11 p.m. in the Baseline Condition. All reaction times from
the low and high sleep reduction conditions were then
converted into deviations from these means in order to
eliminate the effects of interindividual differences. Mean
deviation scores were then calculated for four different
93
STAGE AT AWAKENING, SLEEP INERTIA AND PERFORMANCE
periods: Awakening; Morning (averaging the 8 a.m. and 11
a.m. sessions for Low Sleep Reduction and the 5 a.m., 8 a.m.,
and 11 a.m. sessions for the High Sleep Reduction conditions);
Afternoon (averaging the 2 p.m. and 5 p.m. sessions); and
Evening (averaging the 8 p.m. and 11 p.m. sessions).
Simple Reaction Time Task (SRTT). Deviation scores for
SRTT were used as the dependent variable in a three way ANOVA
with Condition (REM and NREM), Sleep Reduction (Low and
High) and Period (Awakening, Morning, Afternoon, and Evening)
as factors. We found a significant main effect of Awakening
Condition (REM=15.14; NREM=24.10; F1,6=6.77; p=0.0405)
(Hypothesis A), Sleep Reduction (Low=12.91; High=26.33;
F1,6=7.34; p=0.0352), and Period (Awakening=50.23,
Morning=13.42, Afternoon=6.24, Evening=8.58; F3,18=15.76;
p<0.0001). Significant interactions were Awakening Condition by
Period (F3,18=4.07; p=0.0226) and Sleep Reduction by Period
(F3,18=3.48; p=0.0377).
Post-hoc comparisons for Period showed that the mean
deviation at Awakening is marginally significantly different
from that at Morning (Tukey’s HSD, p<0.10), and
significantly different from those at Afternoon and Evening
(Tukey’s HSD, p<0.05), while no significant differences
among these last three periods could be detected.
Post-hoc comparisons for the Condition by Period
interaction showed that the difference between the REM and
NREM conditions is marginally significant upon awakening
(Tukey’s HSD, p<0.10), while no significant difference was
found for the Morning, Afternoon, or Evening (Table 3).
Table 3
SIMPLE REACTION TIME TASK
Mean Deviation Scores for Awakening Condition (REM/NREM),
Sleep Reduction (LOW/HIGH) and Period (Awakening, Morning, Afternoon, Evening). Main Effects and Interactions.
AC
F1,6=6.77; p=0.0405
Main Effects
SR
F1,6=7.34; p=0.0352
REM
15.14
(15.35)
LOW
12.91
(13.39)
NREM
24.10
(21.90)
HIGH
REM
10.20
(11.38)
20.09
(20.75)
HIGH
26.33
(24.09)
Aw
50.23
(36.92)
Mo
13.42
(12.59)
First Order Interactions
AC by PR
F3,18=4.07; p=0.0226
AC by SR
F1,6=4.44; p=0.0796
LOW
P
F3,18=15.76; p<0.0001
NREM
15.63
(17.27)
32.56
(27.63)
Aw
Mo
Af
Ev
REM
37.12
(25.61)
12.10
(12.55)
2.12
(10.42)
9.24
(16.21)
NREM
63.34
(49.22)
14.75
(14.54)
10.37
(21.06)
7.92
(10.69)
Second Order Interaction
AC by SR by P
F3,18=2.31; p=0.1103
Aw
Mo
Af
Ev
REM
28.35
(19.81)
7.53
(13.81)
-1.14
(10.31)
6.06
(10.61)
LOW
NREM
46.30
(36.74)
-0.08
(6.92)
8.50
(47.33)
7.80
(12.91)
HIGH
REM
NREM
45.90
80.39
(35.61)
(65.76)
16.66
29.58
(15.34)
(24.32)
5.38
12.24
(15.16)
(21.06)
12.43
8.04
(22.41)
(11.93)
Af
6.24
(15.16)
Ev
8.58
(12.78)
SR by P
F3,18=3.48; p=0.0377
Aw
Mo
Af
Ev
LOW
37.12
(26.83)
3.72
(7.32)
3.68
(13.73)
6.93
(10.70)
HIGH
63.14
(50.05)
23.12
(19.28)
8.81
(17.99)
10.23
(16.07)
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CAVALLERO AND VERSACE
Post-hoc comparisons for the Sleep Reduction by Period
interaction showed that the difference between the Low and High
Reduction conditions is marginally significant only at awakening
(Tukey’s HSD, p<0.10), while no significant difference was
found for the Morning, Afternoon, or Evening (Table 3).
Four Choice Reaction Time Task (4CRTT). Deviation
scores for the Four-Choice Reaction Time Task were used as
the dependent variable in a three-way ANOVA with
Condition (REM and NREM), Sleep Reduction (Low and
High) and Period (Awakening, Morning, Afternoon, and
Evening) as factors. We found a marginally significant main
effect of Awakening Condition (REM=11.33; NREM=22.38;
F1,6=4.79; p=0.0713) (Hypothesis A), and significant main
effects of Sleep Reduction (Low=13.02; High=20.69;
F1,6=17.21; p=0.0060) and Period (Awakening=49.59,
Morning=10.33, Afternoon=3.63, Evening=3.88; F3,18=45.37;
p<0.0001). The only significant interaction was Sleep
Reduction by Period (F3,18=3.96; p=0.0247).
Post-hoc comparisons for Period showed that the mean
deviation at Awakening is significantly different from those at
Morning, Afternoon and Evening (Tukey’s HSD, p<0.01),
while no significant differences among these last three periods
could be detected (Table 4).
Post-hoc comparisons for the Sleep Reduction by Period
interaction showed that the difference between the Low and High
Reduction conditions is marginally significant only at Awakening
Table 4
FOUR CHOICE REACTION TIME TASK
Mean Deviation Scores for Awakening Condition (REM/NREM),
Sleep Reduction (LOW/HIGH) andPeriod (Awakening, Morning, Afternoon, Evening). Main Effects and Interactions.
Main Effects
AC
F1,6=4.79; p=0.0713
SR
F1,6=17.21; p=0.0060
REM
11.33
(12.01)
LOW
13.02
(14.28)
NREM
22.38
(20.31)
P
F3,18=45.37; p<0.0001
HIGH
20.69
(16.60)
Aw
49.59
(23.82)
Mo
10.33
(14.12)
Af
3.63
(16.33)
Ev
3.88
(11.26)
First Order Interactions
AC by SR
F1,6=3.16; p=0.1256
LOW
HIGH
REM
8.86
(10.42)
13.80
(13.93)
SR by P
F3,18=3.96; p=0.0248
AC by PR
F3,18=1.07; ns
NREM
17.17
(20.09)
27.59
(21.16)
Aw
Mo
Af
Ev
REM
40.92
(17.55)
4.08
(14.14)
-3.05
(10.94)
3.38
(14.30)
NREM
58.25
(37.53)
16.57
(16.26)
10.31
(23.61)
4.39
(9.87)
Second Order Interaction
AC by SR by P
F3,18=0.70; ns
Aw
Mo
Af
Ev
REM
30.61
(22.41)
4.60
(15.15)
-2.84
(16.06)
3.09
(12.80)
LOW
NREM
47.33
(40.78)
7.59
(12.75)
8.39
(26.27)
5.38
(11.81)
HIGH
REM
NREM
51.23
69.17
(25.56)
(35.58)
3.56
25.55
(14.59)
(24.97)
-3.26
12.22
(8.33)
(25.55)
3.67
3.40
(16.68)
(9.55)
Aw
Mo
Af
Ev
LOW
38.97
(21.15)
6.10
(12.46)
2.78
(19.61)
4.23
(11.78)
HIGH
60.20
(28.76)
14.56
(17.06)
4.48
(15.50)
3.54
(11.82)
95
STAGE AT AWAKENING, SLEEP INERTIA AND PERFORMANCE
F1,6=4.25; p=0.0850) and a significant one in the
Morning (REM=3.56, NREM=25.55, F1,6=6.65;
p=0.0418), (Table 4 and Figure 4).
These results show that when sleep is reduced to about
two sleep cycles, the REM/NREM difference is evident, not
only at awakening, as expected, but also during the morning
and afternoon.
Error Rate
Error rates (number of errors/total number of trials) for the
4CRTT were extremely low for all levels of Awakening
Condition, Sleep Reduction and Period, ranging from a
Figure 2
Mean Deviation Score (ms) and Standard Error
of the Awakening x Sleep Reduction Interaction
for Simple Reaction Time (SRT) and Four-Choice Reaction Time (4CRT) Tasks
50
DEVIATION SCORE (ms)
**
***
45
40
35
30
25
20
15
10
REM
5
NREM
0
LOW
HIGH
SLEEP REDUCTION
SRT
LOW
HIGH
SLEEP REDUCTION
4CRT
Figure 3
Mean Deviation Score (ms) and Standard Error
for Simple Reaction Time (SRT) Task for Each Period
DEVIATION SCORE (ms)
in REM and NREM Conditions Following Low and High Sleep Reduction
120
110
100
90
80
70
60
50
40
30
20
10
0
-10
**
**
REM
NREM
AW
MO
AF
EV
AW
LOW
MO
AF
HIGH
EV
SLEEP REDUCTION
Figure 4
Mean Deviation Score (ms) and Standard Error
for Four-Choice Reaction Time (4CRT) Task for Each Period
in REM and NREM Conditions Following Low and High Sleep Reduction
100
*
90
DEVIATION SCORE (ms)
(Tukey’s HSD, p<0.10), while no significant difference was
found for the Morning, Afternoon, or Evening (Table 4).
At this point, we know that when sleep time is artificially
curtailed, a) waking from NREM generally has a worsening
effect on successive performance than waking from REM does
(Hypothesis A); b) four and a half hours of sleep produces
significantly fewer negative effects than three hours of sleep;
c) the negative effect of sleep reduction is at its maximum
immediately after awakening and then decreases progressively;
and d) greater sleep reduction produces (disregarding final stage
at awakening) the worst performance levels upon awakening.
In order to verify the hypothesis that the difference between
REM and NREM awakenings in the average daily level of
performance increases (or becomes significant) in the High
Sleep Reduction Condition (Hypothesis B), planned
comparisons for the interaction Awakening Condition x Sleep
Reduction were conducted with the following results:
Low Sleep Reduction Condition–no significant differences
were observed between the REM and NREM conditions
in the mean deviation for SRTT (REM=10.20,
NREM=15.63; F1,6=1.49; p=0.2679), and the 4CRTT
(REM=8.86, NREM=17.17; F1,6=2.30; p=0.1797) (Tables
3 and 4);
High Sleep Reduction condition–both SRTT and 4CRTT
revealed significant differences between the REM and
NREM conditions in the mean deviation (SRTTREM=20.09, NREM=32.56; F1,6=16.42; p=0.0067.
4CRTT-REM=13.80, NREM=27.59; F1,6=7.37; p=0.0349)
(Tables 3, 4 and Figure 2).
In general, progressive sleep reduction increases the REMNREM difference; for both tasks (SRTT and 4CRTT) the
difference is not significant, though it does go in the expected
direction when Sleep Reduction is Low and becomes
significant when reduction is High.
In order to verify the hypothesis that in the High Sleep
Reduction Condition performance differences following REM
and Stage 2 awakenings persist during the period that goes
from hypothesized sleep inertia dissipation to successive sleep
onset (Hypothesis C), planned comparisons were carried out
with the following results:
Simple Reaction Time Task (SRTT)
Low Sleep Reduction Condition: no significant differences
between the REM and NREM conditions were observed
for any period considered.
High Sleep Reduction Condition: we found a significant
difference between REM and NREM not only at
Awakening (REM=45.90, NREM=80.39, F1,6=7.15;
p=0.0368), but also in the Morning (REM=16.66,
NREM=29.58; F1,6=7.01; p=0.0381) and in the
Afternoon (REM=5.38, NREM = 12.24; F1,6=6.31;
p=0.0457). (Table 3 and Figure 3);
Four Choice Reaction Time Task (4CRTT)
Low Sleep Reduction Condition: no significant differences
between the REM and NREM conditions were observed
for any period considered.
High Sleep Reduction Condition: we found a marginally
significant difference between the REM and NREM
conditions at Awakening (REM=51.23, NREM=69.17,
80
70
60
50
40
**
30
20
10
REM
0
-10
NREM
AW
MO
AF
LOW
EV
AW
SLEEP REDUCTION
MO
AF
HIGH
EV
96
CAVALLERO AND VERSACE
minimum of 0 to maximum of 0.025 (i.e., from 0 to 1 error out
of 40 trials). The scarcity of the data did not allow any kind of
reasonable statistical analysis. Such a low error rate would
indicate that performance accuracy in this task was not at all
influenced by the experimental manipulation.
DISCUSSION
Our experimental design made it possible to compare the
effects of sleep stage at awakening following different amounts
of sleep without any confounding effect due to either circadian
rhythm or sleep architecture. The lack of differences between
the two Awakening Conditions (REM and Stage 2) in all the
physiological parameters considered, confirmed the soundness
of the initial idea of limiting our comparison to Stage 2 and
REM awakenings.
The lack of a REM/NREM difference in subjective ratings
is not surprising; the resolution power of these measures is in
fact too low to reveal anything different from the obvious
relationship between the amount of sleep participants receive
and their sensations of tiredness.
A methodological issue that should be stressed here, instead,
is the high resolution power of the performance tasks we used;
both are very short in duration but both show significant
decreases after experimental sleep reduction, even when the
total sleep time difference between the Low and High Sleep
Reduction Conditions was under two hours. Our tasks were
short in duration, but highly demanding for the participant,
because Inter-Trial Intervals ranged from 600 to 2000 msecs
and therefore required a high rate of response by the participant.
This result confirms the idea proposed by various authors (e.g.,
Dinges and Kribbs, 1991; Gillberg and Akersdtedt, 1998) that in
order to detect sleep loss deficits, it is not necessary to use very
long tasks because, as Gillberg and Akersdtedt (1998) stated,
“there is no safe duration for a monotonous task,” since sleep
deprivation effects on performance can be observed even during
the first trials of the task.
Another interesting aspect of our results is the apparently
different sensitivity of the two tasks to sleep stage at
awakening effects; the SRTT shows a significant difference
between the Awakening Conditions while the 4CRTT does not.
One might speculate that the relatively higher complexity of
the 4CRTT might partially counteract the adverse effects of
being awakened in NREM, but considering that the p value
(0.08) associated with the REM/NREM differences at
awakening is two-tailed, one should opt for a more cautious
interpretation and attribute the failure to reach significance to a
lack of statistical power.
Our results replicate the finding that sleep reduction can
amplify sleep inertia effects upon awakening (as testified by
the marginally significant difference between the Low and
High Sleep Reduction Conditions for simple reaction times and
choice reaction times). This result, however, cannot be
unambiguously attributed to the amount of sleep reduction; we
cannot, in fact, rule out the possibility of a circadian confound
since the awakening scores were obtained at different times for
3
each sleep reduction condition. More interestingly, the
performance results obtained here tend to confirm the
previously-hypothesized (Scott, 1969) differential effect
exerted by sleep stage at awakening on subsequent
performance. This difference increases with the increase of
sleep loss3. In fact, in the High Sleep Reduction Condition, the
difference between the REM and NREM conditions in the
post-awakening test session reaches (for simple reaction times)
and approaches significance (for four-choice reaction times).
Moreover, when sleep reduction is high, the differential effect
of sleep stage at awakening continues until the morning test
session for the 4CRTT and until the afternoon test session for
the SRTT. This difference cannot be interpreted as a
consequence of the sleep inertia effect since there is
considerable agreement among sleep researchers that sleep
inertia maximum duration is 3-4 hours. For this reason, we
think that our results, provided they are replicated in a larger
sample, should lead to a reconsideration of the elements which
determine a participant’s alertness level throughout the day.
Folkard and Akerstedt (1991), for example, proposed a threeprocess model of alertness regulation, according to which
alertness can be predicted by three parameters: Process S
(sleep pressure, which is a function of the time since
awakening); Process C (representing sleepiness due to
circadian influences); and Process W (which refers to sleep
inertia). Should our results be replicated, the addition of a
fourth component to the model would be in order.
We think that this fourth component, final stage at
awakening, not only exerts a differential influence on
performance within the sleep inertia phase, but also impairs
performance after NREM awakenings following inertia
dissipation, especially where alertness levels following sleep
deprivation/reduction are concerned. Should this receive
further empirical confirmation, the predictive power of this
model could be greatly enhanced.
This greater theoretical precision would be of great practical
value for “sleep managers” (Monk and Folkard, 1992)
planning sleep schedules for people involved in continuous
operations (e.g., astronauts) when complete sleep loss is not a
viable way to manage the situation and sleep inertia after naps
is a latent menace to the efficiency and safety of personnel.
ACKNOWLEDGMENTS
This work was supported in part by grant “60% 1998” from
Ministero dell’Università e della Ricerca Scientifica e
Tecnologica (MURST).
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