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SLEEP PATTERNS IN PRE-ADOLESCENT CHILDREN: AN EEG-EOG STUDY

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(Received November 17, 1967; revision accepted January 17, 1968.)

This work was supported in part by NIH Grant number MH 12219-01.

ADDRESS FOR REPRINTS: (J.J.R.) Department of Pediatrics, University of Florida, College of

Medi-cine, Gainesville, Florida 32601.

324

SLEEP PATTERNS

IN PREADOLESCENT

CHILDREN:

AN

EEG-EOG

STUDY

John J. Ross, M.D., Harman W. Agnew, Jr., M.A., Robert 1. Williams, M.D., and Wilse B. Webb, Ph.D.

From the Departments of Pediatrics and Psychiatry, College of Medicine; and Department of Psychology,

College of Arts and Sciences, University of Florida, Gainesville, Florida

ABSTRAC’F. The typical all-night sleep pattern of

the pre-adolescent male was determined by

ana-lyzing the simultaneous EEG-EOG tracings of 18

healthy schoolboys (range 8 to 1 1 years). The sleep patterns of these boys resembled that of older

sub-jects by the occurrence of a more or less orderly

sequence of sleep stages which spontaneously

shifted from one stage to another. Stability of the

pattern for a given boy was observed in the

consis-tent amount of time spent in each sleep stage and

in the number of sleep stage changes night after night.

When compared with the adult sleep patterns,

pre-adolescent total sleep time was 23 hours longer

with unequal distribution of the added time to

each of the sleep stages. Sleep stages in children are longer in duration than in adults, and the sleep patterns are as stable as that of the adult.

Pediat-rics, 42:324, 1968, CHILDREN, DREAMS, ELECTROEN CEPHALOGRAPHY, SLEEP.

LTHOUGH sleep disturbances in childhood

are reported to be common, the nature and extent of these aberrations are difficult to ascertain. The difficulty has been due to three facts :

(

1

)

the lack of proper scientific methods to study human sleep,

(

2) the at-tempt of those engaged in sleep research to describe normal sleep by studying sleep pa-thology, and (3) the lack of normal sleep data obtained by using adequate scientific techniques. After the division of sleep into stages by Loomis, et al.1 and after establish-ment of the fact that Stage 1 rapid eye movement sleep

(

REM

)

was associated with dreaming by Aserinsky and Kleit-man2’3 and Dement and Kleitman,4’ a

use-ful electrophysiological tool, the simulta-neous all-night recording of the electroen-cephalogram

(

EEG

)

and electro-oculogram

(

EOG

),

became available to describe the typical EEG sleep patterns of human

beings. Thus, a reliable documentation of

the electrophysiologic parameters of normal sleep could be accomplished. Major contni-butions toward describing normal adult sleep patterns were made by Dement and Kleitman,’ Oswald,6 Snyder,7 Jouvet,8 Lairy, et al., Roffwarg, et al.,b0,15 Williams,

et a!., 12,13 and Agnew, et al.,14 Through the efforts of these and other workers, the corn-posite picture of a typical night’s sleep in the male and female adult was established, and in the past decade the clinical useful-ness of the sleeping EEG and EOG has been shown to be an aid in diagnosis, ther-apeutics, and prognostication of sleep

disor-ders occurring in adult humans.

When one considers the fact that 19 to

25% of infants and preschool children have

sleep disturbances,15,16 it is astonishing that this EEG-EOG method has not been

cx-ploited in order to understand them. Both

Illingworth and Grant’8 have complained

of the lack of informative and reliable sleep data in the pediatric literature. Recently the present investigators noted that, during the past 12 years, there were only 11

sleep-oriented papers published in the five lead-ing, general pediatric journals written in the English language,lO1OSS and only one of these papers employed the EEG-EOG

technique.28

It is the purpose of the present

communi-cation to report the typical EEG and EOG patterns of sleep in normal S to 11-year-old

male children and to demonstrate how

(2)

STAGE 0

STAGE I (Descending)

STAGE 2

STAGE 3

EM

ARTICLES 32

STAGE 4

lOOgv1______ 2 SEC.

STAGE REM

REMs

Fic. 1. Modified Dement-Kleitman classification of stages of sleep in 8 to

1 1-year-old boys utilizing the simultaneous recording of EEC and EOG.

Rapid-eye-movements (REM’s) at the bottom of the figure are observed

olily during dreaming and normal slow wave eye movements (EM ) are seen

throughout non-REM sleep.

these data can be utilized to better under-stand sleep disturbances that occur in this age group.

METHODS

Simultaneous all-night EEG and EOG

recordings of natural sleep were obtained

on 18 healthy schoolboys (mean age 9.5

years; range 8 to 1 1 years

)

for four

consecu-tive nights in a sleep laboratory which was carefully controlled and monitored for con-stancy of sound, light, and temperature. All boys had slept away from home and their parents at least once prior to this study, and none of them received medication to induce sleep.

(3)

in-TABLE I

MEAN SLEEP STAGE PERCENTS AVERAGED ACROSS

THREE NIGHTS OF SLEEP FOR EACH SUBJECT

Subject Sleep Stage 41. s .1 4 . 47 . 9 .3 43.3 40.7 45.6 36.8 5 .0 49.4 50.4 50.5 46.0 5 .4 42.9 4..2 47.9 44.2 6.5 3 9.4 9.1 6.2 6.1 8.1 4.3 4.7 7.5 5.8 5.8 6.2 2.6 3.4 5.7 3.6 4.9 7.8 4.6 5.9 1.9 4 18.9 24.8 19.8 14.5 21.1 19.9 17.3 15.9 19.9 15.5 17.4 16.4 14.8 19.2 12.4 15.9 22.9 16.1 17.9 3.1

jects retired to the sleeprooms about 8:00 P.M. and slept undisturbed until they

awoke spontaneously the next morning.

Because of the first night effect,29 in which there are numerous awake periods,

less REM sleep, a delay in onset of Stages 4 and REM, and more frequent sleep stage

-iT----i;

--

;-.-;

-I 0.2 6.5 23 .8 changes, the record from the first night of

2 3

:

6

1.8 0.5

:

#{149} 1 .2

5.6 11.9

:

#{149}

7

:

2 26 .7 19.0

::

#{149} 24

:

laboratory sleep was not utilized in analysis

of these data. The remaining tracings from the next three consecutive nights of sleep were analyzed by identical methods.

Ini-7 0.7 6.S 30 .0 tially, each all-night sleep record was

8

9

10

I 1

1.4 2.2 1.5

2.5

8.2

8.5 4.8

2.9 21 .4 26 .7 20.4

21 .6

marked into 1-minute epochs, and each

1-minute epoch was scored using the

fol-. . . .

lowing criteria for epoch classification.

12 13 0.9 0.3 4.0 3.3 25.8

27.6 Stage 0

14

15

16

17

4.I 0.7 4.1

0.3 2.1

6.4 6.2

4.6 22 .8 24 .5

26.0

19.3

Epoch composed of at least 30 seconds of

8 to 12 cycles per second

(

alpha waves

)

of

. . . . . . .

occipital activity with a minimum

amph-18 1.9 6.9 22 .6 tude of 20 p.V. This represents a waking,

--

-

----

resting, eyes-closed state.

Mean 1.5 6.1 24.3

Standard Stage 1

(leviation 1.2 2.5 3.2

-

-

----

-

---structions and preparation. Fifteen Grass

E-1 silver disc electrodes were applied to the subjects’ heads, according to the Inter-national Ten-Twenty System, on F1, F2, F7,

F8, C1, C2, C5, C6, P1, P2, T,, T0, 03, 04, and

ozPz

(

halfway between O and P2

)

. Each electrode was filled with a mixture of ben-tonite paste and Cambridge electrode jelly and was secured to the scalp with collodion saturated gauze pads. Two additional

elec-trodes were applied 1 cm above the outer canthus of the right eye and 1 cm below the outer canthus of the left eye. Eight EEG

recordings between F,-F7, F2-F8, C1-C5,

C2-C6, P,-T5, P2-T6, O3-OP, O4-OP. and

two EOG tracings between left outer

can-thus-right outer canthus, and left outer canthus-F7 were obtained on a 12-channel Grass Model VI electroencephalograph

which was run continuously throughout the night at a paper speed of 15 mm/second and which was calibrated at 50 p.V/5 mm.

With a technician in attendance, the

sub-.

Epoch contained less than 30 seconds of 8

to 12 cycles per second of 20 p.V occipital

ac-tivity and no more than one well defined

spindle or K complex.

Stage 2

Epoch contained at least two well

de-fined sleep spindles or two K complexes, or

one of each, and no more than 12 seconds of .5 to 3 cycles per second 20 tV or greater

slow waves.

Stage 3

Epoch contained at least 13 seconds of .5 to 3 cycles per second 20 &V or greater

activ-it>’, but less than 30 seconds of this activity.

Stage 4

Epoch contained at least 30 seconds of .5

to 3 cycles per second 20 p.V or higher slow waves.

Stage REM

A Stage 1 EEG plus evidence of conju-gate rapid eye movements. This activity

(4)

con-‘rABLE H

PERCENT OF TIME ONE SLEEP

STAGE FouowED ANOTHER

ARTICLES 327

tamed conjugate eye movement until the

eye movements terminated. Any

interrup-tions were subtracted. This is the dreaming

state.

These stages are shown in Figure 1. The

criteria for the five sleep stages are based on the EEC scoring criteria described by Dement and Kleitman,4 Williams, et al.,12,13

and Dement.3#{176}

After scoring for stage of sleep, each epoch of wakefulness and each epoch of

the various stages of sleep were recorded on a score sheet, giving a pictorial

histo-gram and making it possible to calculate

total sleep time, the number of minutes

spent in various sleep stages, the percent-age of total time for the five stages of sleep, sleep latency, sequence of sleep stages, and frequency distribution of the sleep stage

durations.

RESULTS

Overall Sleep Pattern

Using the onset of the first Stage 1 as the beginning of sleep and the beginning of the first prolonged Stage 0 in the morning as the termination, the average total sleep

time for these pre-adolescent schoolboys

was calculated to be 565 minutes (9.41 hours

)

with a range of

483

to 596 minutes

(8.05-9.93 hours). In general the sleep was

continuous except for occasional brief

awakenings as indicated by the occurrence

of a Stage 0 EEG pattern. Upon falling asleep, the boys’ EEC’s demonstrated a

more or less cyclic pattern which sponta-neously shifted back and forth from one stage to another. Initially most subjects moved rapidly through Stages 1, 2, and 3, reaching Stage 4 in 18 minutes and remain-ing in Stage 4 for an average of 42 minutes.

Stage 4 then gave way to Stages 3 or 2

(

Table II

),

after which a brief epoch of Stage 1 accompanied by bursts of

bilater-ally synchronous, conjugate, rapid vertical and horizontal eye movements

(

REM’s)

appeared. During the night the EEC rec-ord showed the cyclic pattern was re-peated four to five times with decreasing

amounts of Stage 4 and increasing amounts

This sleep stage

0 1 2 3 4

Was followed by this sleep stage

0 0.0 10.2 5.7 1.1 1.2

I 80.9 0.0 53.4 2.5 3.2

2 19.1 89.8 0.0 39.1 27.2

3 0.0 0.0 40.9 0.0 68.3

4 0.0 0.0 0.0 57.2 0.0

of REM sleep

(

Table III

)

. Two outstand-ing characteristics of this sleep pattern

were the occurrence of Stage 4 sleep,

pre-dominantly during the first third of the night, and the almost exclusive occurrence of REM sleep during the last two thirds. of

the night. When sleep was moving to deeper and toward lighter stages of sleep, the EEG change from one stage to the next

was smooth and regular, that is, the change

involved a movement across one stage at a

time. This represents a distinct departure from adult patterns when there are abrupt movements across several stages at a time

as the EEC moved toward lighter sleep

stages.

Percent of Total Sleep Time for Each Sleep Stage

Because each sleep stage does not appear at the same absolute time night after night for each subject, it was elected to

investi-gate the amount of time each boy spent in each sleep stage during the three sleep nights. In Table I are the mean percentages

of total sleep time for the five stages of sleep taken across three nights for each

subject. These percentages were obtained by adding the minutes spent in each sleep stage for three nights and dividing by the

total sleep time for three nights and con-venting to a percentage.

From these data it is evident that there

(5)

TABLE III

I)isrRIBLTI0N OF SLEEP STAGE AMOUNTS WITH

RESPECT TO THIRDS OF THE SLEEP PERIOD

Steep

Stage

I! ill

0 26.5 14.5 59.0

1 41.0 33.9 25.1

REM 6.0 33.6 60.4

2 26.4 40.8 32.8

3 55.7 26.5 17.8

4 77.5 18.2 4.3

total time spent in each stage of sleep. For example, Subject 5 spent 29.3% of his sleep in Stage 2, while Subject 15 spent 52.4% in Stage 2. In contrast to Stage 2, Stage 4 only had a range of 12.4 to

24.8%

and REM had a

range of

19.0

to 30.0%. In spite of these indi-vidual variations, it is particularly interest-ing that each subject maintained approxi-mately the same percentage of total sleep for each sleep stage from night to night. The mean percentages of the sleep stages and their standard deviations are shown at

TABLE IV

I)IMTuIHuTI0N OF SLEEL’ STAGE LENGTHS FROM

RECOHI)S REDUCED TO 483 MINUTES IN LENGTH

the bottom of Table I. They represent the average amount of time spent in each sleep

stage across 54 nights and thus indicate what

can be expected in the pre-adolescent boy.

Sequence of Stages

As mentioned before, the EEC’s of this group of subjects spontaneously showed cyclic shifts back and forth from one stage

to another. In Table II( a 5 X 5 contin-gency table) the frequency with which one stage followed another is presented. In 80.9% of the time Stage 0 (waking) is fol-lowed by Stage 1, and 19.1% of the time it is followed by Stage 2. Stage 1 is followed by

Stage 2 89.8% of the time. Stage 2 appears to be primarily a transitional stage because it is followed by Stage 3 only 40.9% of the time and Stage 1 approximately 53.4% of the

time. Stage 3 is followed by Stage 4 only

57.2% of the time and by Stage 2 about

39.1% of the time. These data demonstrate

the general trend seen in older age groups that, when sleep is moving toward Stage 4,

it involves a movement of only one stage at a time. However, absent in these data is the trend found with older subjects to lighten sleep rather abruptly, involving a jump of more than one stage. Rather, the sleep of these pre-adolescent boys is quite regular and smooth when moving to deeper or to-ward lighter stages of sleep.

Table II also demonstrates that the sub-ject does not enter slow wave sleep

(

Stage

3 or 4) without passing through the transi-tional Stages of 1, 2, or 3, that is, one does

not go directly from the waking state into

slow wave sleep. Of almost similar consis-tency, upon leaving Stage 4 the subject

rarely wakes up.

Another important observation is that REM sleep is almost always preceded by Stage 2. Again, the transitional stages

ap-pear important in preparation for the bio-logically significant Stages 4 and REM.

Distribution of Sleep Stages Throughout the Sleep Period

Experience with older age groups has

shown that Stage 4 tends to appear in the first third of the night and REM sleep is

Sleep Stage 0 1 I)uralion (Minutes) 80-84 75-79 70-74 65-69 60-64 55-59 50-54 45-49 40-44 35-39 30-34 25-29 20-24 15-19 10-14 5-9 1-4 Sum 2 5 9 7 7 19 25 36 33 50 61 56 69 134 151 665 3 5 21 113 294 433 4 2 3 2 ii 12 12 ii 17 22 26 19 27 44 36 247 3 3 4 4 11 16 15 25 22 24 28 34 43 53 206 491 1 0 0 0 l 0 0 0 I 1 1 6 81 92 REM 6 3 a 5 15 19 20 25 18 29 32 26 9 4 217

(6)

lour

49

42

30

39

37

33 32

45

37

35

40

23

28

36 30 ‘39

32

43

ARTICLES 329

concentrated in the last two thirds of the sleep period. To demonstrate a similar ten-dency in this group of boys, each of the 54 records was divided into thirds. The

amount of sleep in each sleep stage for the

first, second, and last thirds of the sleep

pe-nod was calculated, and the percent of the

total amount of each sleep stage was corn-puted for its occurrence within each third of the tracing.

Table III shows the percent of the total amount of sleep in a stage which occurred

in each third of the sleep period across all records. It is shown that, during the first third of the sleep period, 77% of total Stage 4 and 56% of total Stage 3 were seen while

only 6% of the total REM sleep was

ob-served. During the last third of the sleep period, the relationship is reversed, with

60% of the REM sleep appearing during this period and only 4% of total Stage 4 and 18% of total Stage 3. The middle third of

the period is characterized by the greatest

heterogeneity of the sleep stages. Worthy

of note is that the transitional stages of 1

and 2 have a fairly even distribution over

the entire sleeping period.

Duration of Sleep Stages

Table IV shows the frequency distribu-tion of the duration of each sleep stage

epoch for three nights of sleep. Each record

was reduced in length to that of the

short-est record (483 minutes

)

. By tallying the

length of each epoch of sleep, it is found

that 68% of the epochs were 19 minutes or

less. If one further reduces the length of

the records to 353 minutes in order to corn-pare with young adults

(

20 to 30 years of

age

)

,

the two groups give approximately

the same distribution of sleep stage lengths. The brevity of the epochs demonstrates the

changeable nature of sleep and shows why

it is difficult to produce a typical sleep

stage histogram.

Number of Sleep Stage Changes

Table V shows the number of sleep stage

changes each night by subject. In order to

permit comparison of this variable between these subjects, all records were reduced in

length to that of the shortest tracing in this age group

(

483

minutes ). As with the stage

amount variable, there are marked differ-ences between individuals in the number of times they change from one stage to an-other. Over the 54 nights of sleep, the num-ber of sleep stage changes ranged from 19 to 56 per night, with a mean of 35.7. There is no consistent pattern either to increase or de-crease the number of changes during the

study; however, there is a tendency for

sub-jects with few sleep stage changes per night to continue to have few changes and for subjects with a large number of changes to continue to change stages frequently. For

instance, Subject 18 had 56, 36, and 43 changes over three nights, which is

consis-tently above the mean, while Subject 12 had 32, 24, and 23 changes, which is consistently below the overall mean of 35.7 changes.

DISCUSSION

Within the past 10 to 12 years, knowledge

of sleep has advanced from the erroneous

‘FABLE V

NuInF:1t (IF SLEEP STAGE (IIAsoF IN RECORDS

REDUCED TO 483 MINUTES IN LENGTH

Night

Subject

H

- ---- -

-Tu’o Three

I 33 42

‘2 30 34

‘3 45 . 33

4 35 29

5 44 43

6 47 23

7 44 28

S 36 38

9 4! 41

10 32 2.5

II 52 32

12 32 24

13 30 29

14 31 26

13 35 19

16 49 38

17 34 29

Is 5(; 36

IeIIII 39.2 ‘31.(;

i!ean

41 .3

35.3 36 .(1 34.3

41 .3 34.3

34.7

40.7

39.7

30.7

41 .3

6.3

29(1

31 .0

25(1

42(1

31.7

45.0

(7)

330

concept of an unconscious suspension of

life punctuated by dreams to the general agreement that it is one of the primary ne-cessities of life, serving both biological and

psychological needs and consisting of

two qualitatively and quantitatively dis-tinct states which differ in their physio-logical properties. Non-rapid-eye-movement

(

NREM

)

sleep, which consists of Stages 1,

2, 3, and 4, occupies the greatest part of

sleep and is characterized in the EEG by

the presence of slow waves and sleep

spin-dies. The biological object of NREM sleep,

though not well understood, probably has something to do with physical recuperation and the maintenance of physiochemical homeostasis. This idea is based on several facts :

(

1

)

non-REM sleep almost always precedes REM sleep on an ordinary night,

(

2) the interval between sleep onset and the first REM period of the night tends to be longer than usual when the individual is

very tired or has stayed up unusually late,1#{176}

(

3

)

children have an unusually long latency to the first recorded REM period starting about the time they discontinue their after-noon naps,1 and

(

4

)

trained athletes who have a vigorous afternoon of training or

contesting demonstrate an increased

amount of slow wave sleep.’ REM sleep is described as a distinct and regularly occur-ring psychophysiological state within the

night sleep cycle during which inward thought, consciousness, and dreaming oc-curs. The well known sleep patterns of high voltage slow waves and sleep spindles are replaced during REM periods by a low voltage, irregular pattern which is very sim-ilar to that of the activated waking state. REM periods occur at intervals of about 90 minutes and constitute 20 to 24% of total sleep time in the adult human. Dement has proposed that there is a need for a certain amount of dreaming,3233 and Fisher and Dement have suggested that dreaming may provide a necessary discharge for

instinc-tual tensions which cannot be gratified in reality.3 When awakened during REM pe-nods, subjects recall dreams in marked de-tail in 80 to 90% of the awakenings. Of

equal interest and significance are the physi-ological changes that occur during REM sleep. In contrast to NREM sleep, REM

sleep is accompanied by: an irregularity and increase in respiratory rate,3 an iregu-larity and increase in pulse rate,35’3 an ir-regular fluctuation and increase in systolic blood pressure,373s an increase in oxygen

consumption rate,3#{176}a decrease in the num-ber of spontaneous galvanic skin re-sponses,4#{176} bruxism,41 fine body movement,40 loss of muscle tone in some muscle groups,42 and penile erections.

Williams, et al.12,13 have shown in young adult males and females that an individual tends to spend a characteristic amount of

time in each sleep stage. They demon-strated that the percent of total sleep occu-pied by each of the four NREM sleep and the REM sleep stages and the number of sleep stage changes were so stable that a

change of 15% in any one sleep stage

ob-tamed in one night equaled one standard deviation from the sample mean. They

con-eluded that the sleep of any particular per-son showed a highly consistent pattern from night to night. However, individual differences were normally present. Data by Williams, et ai.12,13 20 to 30-year-old, adult males and females showed: Stages 0

and 1 occupied 1% and 5%, respectively, of total sleep time; Stage 2 occupied 48% of sleep time and was fairly evenly distributed

throughout the night; Stage 3 consumed only 8% of sleep; and Stage 4 sleep

occu-pied 13% of total sleep time and tended to appear in the first third of the night, while REM sleep occupied 24% of the total sleep time and appeared more frequently in the last third of the night.

When the sleep stage percentages of our pre-adolescent boys

(

S to 1 1 years

)

were compared statistically

(

t-test

)

with those percentages presented by \Villiams, et al.12

on 20 to 30-year-old males, there were no sig-nfficant differences between the two

(8)

percent-‘FABLE VI

MEAN NUMBER OF MINI’TES SL’ENT IN EACh STAGE

OF SLEEP BY Two (;ROIPS OF SIBJECTS

Pre..1do1e.eenf., }‘owi/ .I!iui,te (8-I 1 yr) 2()-.0) jjr) Difference

.S1(I’J(’ .

--

J’re-.ldolen-C;; .lIu,ule,, .iIt.,i!t’: centx-.ldult.,

0 1.5 5.3 0.9 :1.4 3.1

I 6.1 31.5 5.3 I.I 13.1

11E\1 4.3 137.6 4.I 1)1)6 35.0

44. 49J) 48.7 195.3 .51.6

3 5.9 33. 1 7.7 3I .3 IS

4 17.9 101.2 13. 53.8 47.4

Siini 99.9 5(11.5 1)1)9 407.S 157.1)

‘FABLE \lI

1)IMTRIBUTION OF ABNORMAL SIEEe STAGE

PERCENTAGES ASSOCIATED WITh I)ISEASE

Normal Ilyper- .4,,-Pre-.4doler’cent thyroid- orexia Sleep Value,, jsn ‘ervooa .‘t(Ije. -.- ---.. . I Ijoy, Girl,

(C .1).

10yearn I.. yf(?,

(1 I 1. 3 1

I 6 ‘2.5 :

IIESI li 3. 14 I))

44 6.5 l0 52

:t 6 1.9 15 K

4 IS 3. 1 0)

3+4 l4 3-I 31

ilyoteru,

Girl, Girl. Id yenra 12 ycar.

0 11

4 1

l0 17

32 29

6

17 34

43 40

ARTICLES

aM

age comparison. Table VI avoids some of

the difficulties in a percentage comparison

by comparing the mean number of minutes

that our pne-adolescents spent in each sleep

stage to that obtained by the adults. The

younger group was observed to sleep 157

rninutes

(

23 hours

)

longer than young adults. It is also found that this additional

sleep time was not equally distributed to each of the stages. On the basis of an

hy-pothesis that an increase in sleep length is

distributed equally to each stage, one

rould expect a 26-minute increase in the

minutes of sleep in each stage for the

pre-adolescent boys. These data do not support this notion. Fifty-two minutes of the

addi-tional sleep time was distributed to Stage 2,

47 minutes to Stage 4, and 38 minutes to

REM. That this additional Stage 4 sleep

time is a function of the age of the subject

and not the additional sleep time is

sug-gested by a recent, unpublished study. A

group of 17 to 19-year-old subjects who

ha-bitually slept 9 hours or more were studied.

This group of subjects averaged 573 minutes

total sleep time, which is slightly more than

these pre-adolescent males. However, they

obtained only an average of 71 minutes in

Stage 4 sleep, which is 31 minutes less than

that obtained by the subjects of the present

study. Thus, although the pre-adolescent

males do sleep longer than the young

adults, there is evidence to suggest that the

relative great Stage 4 amount is a function

of their age and not of the sleep length.

Upon comparing the mean number of

sleep stage changes per night of the

pre-ad-olescent boys

(

35.7

)

in Table V to the mean number of sleep stage changes in young

adult males

(

35.9

),

there is no significant

difference. However, if one reduces all of

the pre-adolescent boys’ records to 353

mm-utes, vhich is the shortest record in the

adult normal data, the mean number of

sleep stage changes is 28.2, which is

signifi-cantly less than the 35.9 changes observed in

an identical record length for the young

adults. These comparisons suggest that

youthful sleep patterns over the night are

as stable as that of the young adult, but that

the sleep stages in children are longer in

duration. Table IV also demonstrates this.

The data presented by Williams, et

al.,12,13 Agnew, et al.,14 and the present

au-thors reveal that there are some aspects of

sleep which are typical of an individual and

others that are common for human sleep.

Typically, intra-subject stability and consis-tency was observed in the amount of time

spent in each sleep stage and in the number

of sleep stage changes night after night,

while inter-subject similarity of individuals

8 to 60 years of age is observed in the

occur-rence of a more or less cyclic pattern of

sleep stages which spontaneously shifts

from one stage to another, but in which

Stage 4 occurs predominantly in the first

part of the night and REM sleep in the

(9)

quan-titative and reproducible EEG-EOG

mea-surements, a substantial body of data about

children and adults is provided as an

effec-tive frame of reference against which

path-ological deviations may be evaluated.

Although much of an authoritative na-ture is written about sleep problems in chil-dren, there has been scant documentation of electrophysiologic alterations in sleep

pa-rameters. During the past year this

labora-tory had the opportunity to perform EEC-EOG studies on several pre-adolescent chil-dren with the following medical and

psy-chiatric illnesses : hyperthyroidism, anorexia nervosa, and hysteria (Table VII

)

. The

patient with hyperthyroidism was a

10-year-old boy with typical signs and

symptoms of Crave’s disease, including

fret-ful sleep with frequent body movements, emotional disturbances, and diminution in school performance. On his initial hospital-ization at the University of Florida

Teach-ing Hospital, the EEG-EOC all-night sleep

recording showed a marked deviation of his sleep pattern from normal means. Stage 4

sleep occupied 39% of total sleep time,

which is about seven standard deviations

above the mean value for his group, and

REM was 14%, which is about three stan-dard deviations below the mean value. Of

particular interest to us was the return of

his percentage sleep stage values to normal

as he received appropriate treatment with

propylthiouracil and desiccated thyroid.

Our 12-year-old girl with anorexia nervosa also showed an abnormal sleep pattern dur-ing her hospital investigation. Particularly

noteworthy was the 10% REM value which was four standard deviations below the

mean value of 24% for the pre-adolescent

age group as well as a Stage 4 value of 26%.

Table VII also presents the sleep patterns of two other patients-one, a 12-year-old girl who was admitted for headaches, poor

school performance, insomnia, enuresis, hal-lucinations, and transient hemiparesis and who was diagnosed as having a psychoneu-rotic reaction with a hysterical personality. Another 12-year-old girl was admitted with

headaches, brief “lapses,” screaming and

kicking spells during which she threatened to kill somebody, insensitivity to pails over

half of her body, and tunnel vision on the

same side. The latter patient was thought

to have conversion hysteria. Of interest to us

was the finding in both of these girls of the

marked increase in total sleep time spent in Stage 4 sleep and the mild depression of

REM sleep. We have not had the

opportu-nity to retest the three girls to date.

The authors are not prepared to offer an

explanation for the divergent sleep

pat-terns. We have no idea whether the organic

and emotional illnesses are responsible for the abnormal patterns or whether abnormal

sleep patterns cause emotional

distur-bances. Abundant data from the electroen-cephalographic, endocrine, and sleep areas

effectively demonstrate that variations in the human sleep pattern can result from drugs,45-48 disease,#{176}5 and various forms of sleep deprivation

(

total,8 partial,’#{176}#{176}and selective

)

33,61-63 The only point we wish to

make is that patients with severe medical

diseases, some of whom have marked sleep

disturbances, may have abnormal sleep

pat-terns. The significance of this observation

remains for future research to determine.

SPECULATIONS

In the minds of the authors the major

contribution of this research is the fact that it represents the first systematic application of the EEC-EOG methodology and of the modified Dement-Kleitman scoring criteria

to study childhood sleep and sleep distur-bances. Now mere visual observation and

conjecture have been eliminated, and a

safe, effective, convenient, quantitative,

re-producible, descriptive method is available for investigating sleep in children. Since there is so little basic, quantitative data which pertains to childhood sleep, this ap-proach represents an important

break-through in our attempt to understand

dis-turbed sleep in children and a vigorous ap-plication of these methods and concepts should speed a better understanding of

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ARTICLES 333

adults,2,SS61GO and efforts to correct them

are being attempted.7 In children it

ap-pears to us that the measurement of percent

of total sleep time spent in the five sleep stages is a sensitive indicator of the electro-physiological characteristics of sleep, and

investigation of this measurement may

make it possible to gain an understanding

of the intra-sleep, medical, and psychiatric

disorders of sleep.

SUMMARY

Simultaneous all-night EEG and EOG

recordings have been shown to be an

effec-tive, quantitative, and reproducible method for studying children’s sleep. Application of a modified Dement-Kleitman scoring tech-nique to the 54 records obtained from 18 healthy, pre-adolescent boys made it

possi-ble to describe quantitatively their typical sleep pattern. Descriptive measurements

in-eluded: percent of total sleep time spent in

each stage of sleep, total minutes in each stage of sleep, sleep duration, sleep latency, sequence of sleep stages, distribution of

sleep stages throughout the sleep period,

duration of sleep stage epochs, and number of sleep stage changes. Although individual variations are apparent, it was found that

each boy maintained approximately the same percentage of total sleep for each sleep stage from night to night. First ex-perience utilizing this clinical all-night EEG-EOC tool in children suggests this technique should permit a higher yield of

significant scientific data in the study of

sleep problems.

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1968;42;324

Pediatrics

John J. Ross, Harman W. Agnew, Jr., Robert L. Williams and Wilse B. Webb

SLEEP PATTERNS IN PRE-ADOLESCENT CHILDREN: AN EEG-EOG STUDY

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1968;42;324

Pediatrics

John J. Ross, Harman W. Agnew, Jr., Robert L. Williams and Wilse B. Webb

SLEEP PATTERNS IN PRE-ADOLESCENT CHILDREN: AN EEG-EOG STUDY

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