The Cyclic Alternating Pattern as a Physiologic Component of

Sleep, 8(2): 137-145
© 1985 Raven Press, New York
The Cyclic Alternating Pattern as a
Physiologic Component of Normal
NREM Sleep
M. G. Terzano, D. Mancia, M. R. Salati, G. Costani,
A. Decembrino, and L. Parrino
Clinica Neurologica dell' Universita di Parma, Parma, Italy
Summary: The cyclic alternating pattern (CAP) is a long-lasting periodic activity
consisting of two alternate electroencephalogram (EEG) patterns. This variation
in EEG is closely related to fluctuations in the level of arousal that characterize
two different functional states in the arousal control mechanism. We studied 20
sleep records of 10 healthy subjects to see if CAP appears under physiologic
conditions. During NREM sleep, CAP corresponded to a periodic succession of
spontaneous phasic phenomena recurring within every stage, i.e., intermittent
alpha rhythm, K-complex sequences, and reactive slow wave sequences. The
following analyses were performed. Each EEG specific alternating pattern, defined
as a cycle, was subdivided into two phases depending on the arousal response to
stimulation. Average cycle length, average duration of each phase, and average
ratio phase/cycle were calculated. CAP rate defined as (CAP time/Sleep time)
was calculated for total sleep time (TST), (CAP time/TST); for NREM sleep,
(CAP time/Total NREM); and for each NREM sleep stage. CAP is the EEG
translation of the reorganization of the sleeping brain challenged by the modification of environmental conditions. Key Words: Cyclic alternating patternSleep organization--Coma and sleep--Adjustment systems.
Trace altern ant or cyclic alternating pattern (CAP) is characterized by the regular alternation of two electroencephalogram (EEG) patterns and represents a complex form of
periodic activity (l,2). Clinically, CAP is a most useful EEG feature in the diagnosis of
posttraumatic and other causes of coma (3-6).
As we reported previously (2,7 ,8), CAP may be subdivided into two phases, depending
on the arousal response to stimulation. Phase A and the following phase B, which compound
each cycle of CAP, respectively, correspond to levels of greater and lesser arousal. Therefore,
when CAP appears, arousal fluctuates constantly between two distinct steep levels. This
modulation of arousal affects not only EEG but also autonomic, muscular, and behavioral
functions, which increase during phase A and decrease during phase B (3,8).
Accepted for publication December 1984.
Address correspondence and reprint requests to Dr. M. G. Terzano at Clinica Neurologica dell'Universita di
Parma, Strada del Quartiere 4,43100 Parma, Italy.
137
138
M. G. TERZANO ET AL.
Since CAP is present in pathologic conditions, it is reasonable to assume that its mechanisms might also operate under normal conditions, including the operation of arousal
control during sleep. The purpose of this article is to identify, in the organization of normal
sleep, the existence of an EEG pattern with the specific reactivity of CAP and to determine
the temporal features of this pattern. Hypotheses based on the cybernetic model of reciprocal
induction are presented to analyze CAP function (9).
METHODS
Ten healthy subjects with no sleep complaints volunteered for our study [5 men and 5
women, aged 20 to 30 years (mean 24 years)]. They all slept for 3 consecutive nights in
an air-conditioned, partially soundproofed sleep laboratory at Parma University Department
of Neurology. Time in bed (TIB) was 500 min long.
The recordings were monitored with a Reega Alvar Duplex TR XVI polygraphic apparatus
using 10 bipolar leads (Fp2~F4, F4-C4, C4-P4, P4-02; Fpl-F3, F3-C3, C3-P3, P3-01; FZCZ, CZ-PZ), an electro-oculogram (EOG), and an electromyogram (EMG) of the mentalis
muscle. An electrocardiogram (ECG), a pneumogram (PNG) through mouth and nose, and
an EMG of a deltoid muscle were also conducted.
The EEG reactivity was assessed during night 1 by means of acoustic and visual stimuli.
Sounds and lights were produced either separately or synchronously by a hand-controlled
Sone~lat-TR Alvar stimulator. Light stimulation, 0.3 J at the source, was produced by a
stroboscope placed 20 cm from the subject's face. The acoustic stimuli ranged between 50
and 5,000 Hz and between 30 and 90 dB. Two loudspeakers were placed 30 cm from each
side of the subject's head. Each morning all subjects completed a questionnaire that included
a subjective assessment of the quality of sleep.
DATA ANALYSIS
Only data obtained from nights 2 and 3 were analyzed. Two EEG readers, exhibiting a
high degree of interscorer correlation, scored the records separately.
All segments characterized by the cyclic alternation of two different EEG patterns and
by simultaneous variations of one or more polygraphic parameters (presence or absence of
eye movements and phasic muscular activities, increased or decreased cardiac and respiratory
frequency and muscle tone) were selected. Each cycle that included these two EEG/polygraphic patterns was identified as CAP. Throughout sleep, these cyclic changes could be
found in isolation, but only CAPs clustered in sequences including at least two consecutive
cycles were scored. Localized, slow, high-voltage waves, random K-complexes, and periodic
isolated K-complexes were not included.
During night 1 the intensity and the type of stimuli were intended only to evoke an EEG
response, and therefore no inferences were made concerning sensory and arousal thresholds.
Depending on the response to stimulation, two arousal levels of CAP were differentiated.
When a sufficiently intense s.timulus was applied during CAp, one of the two cyclic patterns
(called phase B) always changed into the spontaneous features of the other CAP component
(called phase A). Stimuli of any intensity and type applied during phase A never caused
the appearance of an EEG pattern peculiar to spontaneous phase B. Thus, phase A was
considered the greater arousal level and phase B the lesser arousal level (Fig. 1).
Sleep stages were differentiated according to standard criteria (10). For each sleep stage,
CAP was identified as follows: in stage 1, phase A corresponded to alpha activity and
phase B corresponded to its disappearance (Fig. 2); in stage 2, phase A consisted of KSleep. Vol. 8, No.2, 1985
139
CYCliC ALTERNATING PATTERN IN SLEEP
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FIG. 1. Cyclic alternating pattern (CAP) reactivity during sleep as a result of acoustic stimulation. This is
characterized by a 1,000 Hz pure tone lasting 250 ms of 40-dB intensity. Arrows indicate the limits of consecutive
phases A and B. When the stimulus is applied during phase A (greater arousal), electroencephalogram (EEG)
changes are very slight. When the same stimulus is applied during phase B (lesser arousal), EEG immediately
changes into the spontaneous pattern of phase A. Oculog., recording of eye movements; EKG, electrocardiogram;
EMG, electromyogram; PNG, pneumogram.
complex sequences with a persisting 8- to 12-Hz alpha-like component and phase B consisted
of the background rhythm peculiar to that stage (Fig. 3); in stage 3, phase A consisted of
K-complex sequences and of reactive slow waves, the reactivity of which was similar to
that of K-complexes (11), and phase B consisted of the background rhythm peculiar to that
stage (Fig. 4); in stage 4, CAP had the same characteristics as in stage 3 (Fig. 5).
In REM sleep, the EEG hardly varied, and the spontaneous changes in the autonomic
functions were rather irregular. It was not possible, therefore, to identify a pattern similar
to CAP in this stage.
The following CAP parameters were calculated: (a) average cycle length; (b) average
duration of each phase; (c) average ratio phase/cycle, as: Phase A rate = (phase A duration!
cycle duration) X 100, and phase B rate = (phase B duration!cycle duration) X 100; (d)
CAP index, expressed as the number of CAPs per minute of NREM stages, as:
OCUlOG -
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sO.uv
FIG. 2. Cyclic alternating pattern (CAP) in stage 1 recorded through 13 electroencephalogram (EEG) bipolar
leads. Phase A corresponds to the trace with alpha activity. Phase B corresponds to the trace with lower voltage
and with no alpha activity. Oculog., recording of eye movements; EKG, electrocardiogram.
Sleep, Vol. 8, No, 2, 1985
M. G. TERZANO ET AL.
140
OCULOG -
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1 Sec
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FIG. 3. Cyclic alternating pattern in stage 2. Phase A corresponds to the K-complex sequences and alpha
activity. Phase B corresponds to the low-voltage trace with spindles. Oculog., recording of eye movements;
EKG, electrocardiogram.
CAP index-total stage 1-4 =
number of CAPs in stage 1-4
total stage 1-4 time in min
(e) for each sleep record, CAP rate, i.e., (CAP time/sleep time), was calculated for:
total sleep time (TST)
NREM sleep
each NREM total sleep stage
=
total CAP time
TST
x 100
total CAP time
- - - - - - x 100
NREM sleep time
CAP time in stage 1-4
-----~--
total stage 1-4 time -
x 100
Student's t test was used to determine the differences in cycle length and CAP rates, in
CAP index, and in the number of CAP sequences per minute within single sleep stages.
RESULTS
Over the 20 nights of recording, quality of sleep was considered normal in all but three
subjects. Three sleep records included five Dement and Kleitman cycles (12), 16 records
included four, and one record included three.
Table 1 reports the parameters for the 328 CAP sequences appearing in the 20 sleep
records. When the number of CAP sequences per minute was compared with the single
sleep stages, the highest value was found in stage 1 (p < 0.01).
In the classic sleep histogram (Fig. 6), CAP sequences were somewhat related to sleep
stages and Dement and Kleitman cycles. Particularly, CAP sequences were often preceded
and/or followed by some dynamic event of sleep: falling asleep, sleep stage changes, arousal
without waking, -or "phase d'activation transitoire." CAP sequences always appeared in
Sleep, Vol:-8, No_ 2, 1985
CYCLIC ALTERNATING PATTERN IN SLEEP
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FIG. 4. Cyclic alternating pattern in stage 3, Phase A corresponds to the sequences of higher voltage, regular
slow waves, Phase B corresponds to the background rhythm peculiar to that stage, Oculog" recording of eye
movements; EKG, electrocardiogram,
any NREM stage that immediately preceded REM sleep. This peculiar characteristic contrasted sharply with the lack of CAP sequences in the first part of all stage 2 periods that
immediately followed REM sleep (Fig. 6).
The 328 CAP sequences included 2,381 CAPs, 1,578 (66.3%) of which were found in
the first half of sleep and 803 (33.7%) in the second half.
Table 2 reports the values of CAP parameters. The first set of data reports the averages
for each subject, whereas the second set of data reports the overall values for the 2,381
cycles and the CAP rates.
Cycle length could vary, but 83% of CAPs lasted from 10 to 60 s, the average cycle
length lasting about 40 s. Phases A and B were much more variable. If cycle duration was
broken down into the percentage duration of its components, it appeared that phase B rate
was >50% in 75% of the cycles, whereas only in 25% of CAPs did phase A rate exceed
50%. CAP rate accounted for a little less than one-fifth of TST and for a little more than
OCULOG._~~~~~
_ _~_ _ _
1 Sec
--.J
50JJV
FIG. 5. Cyclic alternating pattern in stage 4. Phase A corresponds to the sequences of more regular and
higher voltage activity. Phase B corresponds to the more irregular, lower voltage activity. Oculog., recording
of eye movements; EKG, electrocardiogram.
Sleep, Vol. 8, No.2, 1985
142
M. G. TERZANO ET AL.
TABLE 1. Values of parameters for 328 cyclic alternating pattern
(CAP) sequences
Mean
16.4
Number of CAP sequences for each sleep
Duration of CAP sequences (s)
Number of CAPs in each CAP sequence
Number of CAP sequences in:
Sl (n = 43)
S2 (n = 181)
S3 (n = 28)
S4 (n = 21)
2 stages (n = 51)
3 stages (n = 3)
4 stages (n = 1)
(4.511)
298.2 (82.63)
7.47 (1.82)
2.15
9.05
1.4
1.05
2.5
(1.9)
(2.8)
(1.01)
(1.2)
(1.9)
Range
10--28
201.3-516.6
4.6--11.5
0--9
3-14
0--4
0--4
0--4
Standard deviations in parentheses. CAP, Cyclic alternating pattern; SJ, stage 1;
S2, stage 2; S3, stage 3; S4, stage 4.
one-fifth of NREM sleep time. Total CAP time in each sleep record ranged from 49 min
15 s to 129 min 5 s.
Table 3 reports CAP parameters and CAP rates for each NREM sleep stage. Stage 1
had the longest CAP length (p < 0.01) and CAP rate (p < 0.01). In the same stage the
CAP index was significantly higher than in other stages (p < 0.01).
DISCUSSION
Sleep and wakefulness represent the two physiological extremes of arousal within the
24-h nighUday cycle. These two conditions are controlled by specific neurophysiological
structures and neurotransmitters localized in the brainstem (13-15). However, fluctuations
in the level of arousal occur during wakefulness and sleep. The latter consists of vari()us
V
II
III
IV
REM
TIME
min.
O·
100'
200'
300'
400'
500'
O·
100'
200'
300'
400'
500'
V
II
III
IV
REM
TIME
min.
FIG. 6. Histogram of two consecutive sleep records taken in the same subject. Dotted lines indicate the cyclic
alternating pattern sequences. V = wakefulness; I, II, III, IV, and REM = sleep stages.
Sleep, Vol. 8, No.2, 1985
143
CYCLIC ALTERNATING PATTERN IN SLEEP
TABLE 2. Individual and overall values o/CAPs
Individual values of CAP for
each sleep (20 records)
Range
Mean
Number of CAPs
Duration of cycles (s)
Duration of phase A (s)
PAR (%)
Duration of phase B (s)
PBR (%)
CAP ratelTST (%)
CAP rate/NREM (%)
119.05
39.73
12.66
36.25
27.07
63.74
18.15
23.19
(28)
(4.91)
(2.48)
(4.67)
(4.21)
(4.67)
(4.87)
(5.73)
83-180
29.5-46.2
9.5-17.4
29.9-49.1
18.4-34.3
50.8-70
11.6-28.8
15.13-35.4
Overall values for 2,381 CAPs
Mean
Range
39.95
12.68
36.07
27.27
63.93
18.11
23.16
(22.9)
(9.22)
(17.53)
(19.84)
(17.53)
(4.97)
(5.87)
7-285
2-120
4.58-95.16
2-165
4.83-95.41
10.31-28.8
15.13-35.42
Standard deviations in parentheses. CAP, Cyclic alternating pattern; PAR, phase A rate; PBR, phase B
rate; CAP ratelTST, CAP rate with respect to total sleep time; CAP rate/NREM, CAP rate with respect to
NREM sleep time.
stages characterized by different EEG/polygraphic patterns and by different threshold responses to arousing stimuli (16-18). According to Dement and Kleitman, sleep may be
subdivided into cycles lasting 90 to 100 min (12).
CAP is an additional chronological structure with an average rhythm of its own of about
40 s. This biorhythm may involve not only arousal control but also other biological functions
during sleep such as cerebrospinal fluid pressure, systemic arterial pressure, pulmonary
arterial pressure, heart rate, respiration, diameter of pupils, and excitability of peripheral
neurons (19,20).
Nothing is known about the existence of a pacemaker or of control structures being
directly linked together. Presumably, during sleep all these functions may be simultaneously
involved through a coordinating process controlled by the level of arousal (21). This
synchronized response is called "phasing" (22), and it occurs when arousal is either fluctuating or in a steady state. As in any biological function, a steady state may be achieved
by the application of a bipolar feedback system (9,23,24). CAP may be considered the
bioelectrical translation of such a mechanism. Arousal instability is due to the combined
effects of internal and/or environmental stimuli. Through continuing oscillations CAP would
aim to restore a steady state that may be represented in that moment by the arousal level
of single NREM sleep stages (23).
During CAP the behavior of arousal may be interpreted according to the cybernetic
model of reciprocal induction (9). In conformity with this theory, we may assume that
arousal regulation is controlled by two half-systems dynamically linked together: a greater
arousal inducing system, which initially responds to arousing stimuli and elicits the appearance of phase A, and a lesser arousal inducing system, which initially responds to stimuli
that reduce the level of arousal and elicits the appearance of phase B. The result is a twolevel, fluctuating controlled process appearing on EEG as CAP. Therefore, the afferent
impulses may be selected by the sleeping brain. Generally, if the stimulus were compatible
with the condition of sleep at that moment, then its effects would be offset by CAP
mechanisms; if the stimulus were not compatible with the level of arousal existing at that
moment, then the arousal control system would adjust itself by diverting the resulting effect
onto a different level of arousal. This may be the reason why CAP usually appears at the
time of stage changes, awakenings, and falling asleep.
Sleep, Vol. 8, No.2, 1985
........
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t
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TABLE 3. CAPs in stages of sleep
n = 224 (9.4%), SI
Mean
Number of CAPs for
each sleep
Duration of cycles (s)
Duration of phase A (s)
PAR (%)
Duration of phase B (s)
PBR (%)
CAP index
CAP rate (%)
= 1,615 (67.8%),
S2
n
= 325 (13.6%),
S3
Mean
Range
Mean
Range
80.7 (20.99)
39-128
16.2 (13.79)
0-60
ILl
(9.63)
0-43
54.17
23.07
44.25
31.1
55.74
0.87
56.74
(34.79)
(19.6)
(21.01)
(26.33)
(21.01)
(1.05)
8-285
2-120
4.93-94.68
3-165
5.31-95.06
0-1.7
Standard deviations in parentheses. n
stage 3; S4, stage 4.
n
Range
38.37
11.43
34.78
26.94
65.21
0.33
21.04
(21.62)
(6.96)
(16.93)
(19.68)
(16.93)
(0.09)
7-127
39.29 (18.48)
2-80
11.25 (4.02)
4.58-95.16 34.11 (16.27)
28.03 (18.1)
2-116
4.83-95.41 65.89 (16.27)
0.17-0.59
0.44 (0.26)
31.08
10-116
5-29
8.23-84
4--106
16-91.76
0-0.57
n == 217 (9.2%), S4
Mean
10.8
(8.18)
(16.94)
38
13.34 (5.16)
40.09 (17.05)
24.65 (16.21)
59.9 (17.05)
0.25 (0.22)
15.67
Range
0-25
9-102
6-37
9.85-83.87
3-82
16.12-90.14
0-0.81
2,381. CAP, Cyclic alternating pattern; PAR, phase A rate; PBR, phase B rate; SI, stage 1; S2' stage 2; S3'
~
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CYCLIC ALTERNATING PATTERN IN SLEEP
145
CAP rates might indicate the number of operations that the sleeping brain must perform
to adjust itself to "normal environmental conditions." In conclusion, it might reflect the
flexibility of sleep organization.
Acknowledgment: This work was supported by grants of the Italian Ministry of Public Education
(Ministero della Pubblica Istruzione).
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