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(1)

Changes in

Sleep Spindle and Sleep Slow Wave during the

Cycle

Menstrual

Yoshikazu IsHizuKA

Dopartment ofNeuroPsychiatry, Yamanashi Medical College

Abstract: Five healthy adult women, aged from 20 to 28, had 12-15 polysomnographic

recordings taken. Sleep stages were scored according to the Rechtschaffen and Kales criteria. Cz-Al EEG recordings were also analyzed with a spindle and delta wave real-time automatic analyzing system in a l6-bit microcomputer. Sleep stage analysis revealed no signficantchanges in the ordinary sleep parameters, i.e. percentage of each sleep stage, sleep latency or REM latency when the low and high body temperature phases were compared. On the other hand, the s}eep spindle parameters derived from the Persoltal Spindle Delta-wave Analyzer changed markedly during the menstrual cycle. Spindle frequency was slower at about l4 days before the first menstruation day and increased after that and it was faster atjust before the first menstruation day. The pattem of spindle density change was similar to that of frequency. Amplitude and duration did not tend to change during the menstrual cycle nor did the parameters of the slow wave. No prior reports have mentioned the relationship between the menstrual cycle and sleep spindle. From these results, it can be hypothesized that the frequency ofthe sleep spindle reflects sleep propensity and that it is a very important sleep parameter.

Key words: Sleep, Sleep Spindle, Sleep slow wave, Automatic analysis, Menstrual cycle

INTRODUC ['ION

It is well known that the sleep condition ofa

healthy woman changes during the menstrual

cycle. But details of a woman's sleep condition

are still unknowR. We studied woman's

subjec-tive evaluations of their sleep feeling using a

sleep questionnaire aRd found that subjective sleep feeliRgs change regularly during the meRstrual cyclei). Generally speaking, sleep

feeling in the high temperature phase, tha£ is

two weeks before the menstrual period, is worse than that iR the lew temperature phase. On the other hand earlier studies by many

other researchers using polysomnography

(PSG) have not yet had fruitful results. We caR

now analyze the electroencephalography

(EEG) of PSG more easily than hitherto by means of a persoltal computer. In this study, analyzing the EEG of PSG with a new sleep EEG analyzing system, changes iR the sleep spindle and sleep slow wave during the men-strual cycle were examined.

Tamaho, Yamanashi 409-38, Japan

Received February 26, 1992 Accepted Apri} 8, 1992

SUIljECTS ANP METHODS

Subjects

The subjects were five females who had been iRcluded in our former study of subjective sleep change duriRg the menstrual cyclei). The subjects were one 20-year-old (subject MT), two 22-year-old (subjects MI and HN), one 25-year-old (subject MO) and oRe 28-yeay-old (subject YK). All of them were healthy, their menstrual cycles were regular and had not been pregnant or takeR oral contraceptives.

(2)

Subject MT Subjeet YK Subject Ml Subjeot HN Subieet Me

M

Fig. 1.

-28 -21 -14 -7 e 7

Day of Menstrual Cycle

Schedule of this study

In a period of 35 days from the 28th day before menstruation to the 7th day after

menstruation, polysomnographic record-ings for each subject were done 12-15

times, Each dot incllcates one polysomno-graphic recording. The first day of men-struation is shown as day O in the figures and is marked with an M. The days before menstruation are indicated with a minus symbol.

IRforrned consent was obtained. Methods

Subjects were asked £o live erdinary and Rot

te drink alcohol, take drugs or smoke during

the sttidy.

1) Polysomnographic study and visgal sleep stage scormg

After one adaptatioR night, sleep stv{dies were performed in quiet single rooms in our sleep laboratory. The electroeRcephalogram (EEG), electromyogram (EMG), electrooculo-gram (EOG), electrecardioelectrooculo-gram (ECG) aRd the respiratogram were monitored at the rate of

10 mmlsecond at least three nights a week during a mens£rual cycle. For the EEG, Fpz-Al Cz-Fpz-Al aRd Oz-Fpz-Al leads were used '

ing to the international tenltwenty system. Fer

the EMG, electrodes were placed at a point on the mental muscle; for the EOG, the electrodes were applied to the left and right caRthi. The recordings started about ll:OO p.m.-l2:OO

p.m. according to the ordinary life schedule of

the subjects aRd were terminated compulsorily

eight hours after the start. Twelve PSGs for subjects MT, MO and YK, thir£een for subject HN, and fifteen for subject MI were obtained during a menstrual cycle (Fig. I). PSGs were recorded on paper and magnetic tape simul-taneously. Sleep stages were scered by the Rechtschaffen 8c Kales criteria2). From the

results for sleep stages, the perceRtage of each

sleep stage, sleep la£ency and REM sleep latency were calculated.

2) Measureit}ent of Basal Body Tempera-t"re (BBT)

BBT was measured every morning during

the experimental schedule.

3) Measurement of sex hormone coRceRtra-tioit

Once in the low temperature phase aRd

twice in the high temperature phase, the blood coRcentratieRs of the luteinlzing hormone, fo11icle stimulating hormone, estradiol and progesterone were measured.

4) Autoanalysis of sleep EEG

Cz-Al EEGs, which were recorded on

magnetic tape, were analyzed with a Personal Spindle Delta Analyzer (PSDA) developed by

the Tokyo Metropolitan Institute for

Neurosciences3'4). By means of this analyzing system, spind}e structure, i.e. the density (number per mirmte), duration (msec), ampli-tude (paV) ar}d frequency (Hz) of the sleep spindle, aRd slow "rave structure, i.e. total number, density (Rumber per minUte), ampli: tude (paV) and freq"ency (Hz) ofthe slow wave, can be analyzed. The PSDA consists ofa l6-bit personal computer, l2-bit A!D convertor aRd

sof£ware digital filter. In this study, the sleep

spindle was defiRed as composed of over six waves with a frequency range of 11 to 16 Hz and amplitude greater than 5 uV. The sleep slow wave was defiBed as having a O.5-1.5 Hz frequency aRd over 50 ptV. amplitude.

Follow-ing these definitions, the styucture of the sleep

spiRdle and slow wave were studied in detail during sleep stage 2, 3 and 4 for the entire

night.

(3)

period is shown as day O aBd marked with an M. The X axis is shown from 28 days before to

7 days after the fu"st day ofthe menstr}Jial cycle.

REsuLTs

I) The BBT of all s"bjects showed a

bi-phasic (low temperature phase and high

temperature phase) pattern dm"ing the men-strual cycle and the change iB sex hormones had a normal pattern parallel to BBT. From these yesults, these subjects were judged to have healthy menstrual cycles.

2) Changes in sleep parameters which were scored visually (Table I)

SiRce the time and date of PSG differed from stibject to subject, we selected two PSG

parameters each from the low and high

temperature phases and compared them by

pai}'ed t-test. There were no significant changes iR the percentages of REM sleep, each NREM sleep aRd sleep latency aftd REM sleep

latency.

3) Changes iR the sleep spind}e s£ructure analyzed by means ofthe autoanalysing system Average duration (msec), average amplitude (ptV), deRsi£y (number per miBute) and

aver-age frequeRcy (Hz) were studied statisticaily by

ANOVA for each subject.

The average duration of the sleep spindle of

s"bjects MO and YK did not change

sigRi-ficantly. Though that of subject MI chaRged (F==4.ll), we cou}d not find a relationshjp to

the mekstrual cycle. Those of subject HN

(F =6.87) and subject MT (F= 7.45) changed significantly. There was Ro common pattem of change in the average duration of the spindle during the menstrual cycle seen among the

subjects (Fig. 2a).

The average amplitude of the spindle in subject MO incyeased transien£ly at l4 days before menstruation (F =l4.9). That of HN iRcreased towards memstruation (F=:5.3). That of Ml changed more in the second half of the

menstrual cycle than iR the first half

(F=10.56). These of subjects YK and MT

chaRged significantly, but no change related to

the menstrual cycle could be seen. Although the change in the average amplitude for each

sub.ject was statistically significant, there was

great iRdividual differeRce among change

pat-terns for these subjects and the change pattern

was not necessarily related to the menstrual

cycle (Fig. 2b).

Although the density ofthe spindle differed from subject to subject, the change patterrts which were related to the menstrual cycle were

relatively similar. Trhey increased from 14 days

before meRstruation and then decreased im-mediately before menstyuatioR. The changes were significant (p<O.O05) in ANOVA, the F values for the subjects being as follows:

MO =9.47, HN=8.53, MI=1l.57, YKme12.9

altd MT==6.6, (Fig. 2c).

The average frequency of the spindle

underwent a clear common chaRge in five

Table 1. Changes in sleep parameters in two phases ofthe rr}enstrual cycle

There were no significant changes in sleep parameters in Iow temperature and

phases

high tempel'atLll-e

Low Temperature Phase High Temperature Phases

Sleep Latency (min)

REM Latency (min) % Stage REM % Stage 1 % Stage 2 % Stage 3+4 27.l (28.8) 86.1 (40.0) 22.3 (2.5) 4.5 (2.1) 53.5 (6.4) 19.7 (5.5) 20.8 (13.5) 83.7 (27.5) 21.3 (3.3) 5.2 (2.2) 55.9 (6.4) l7.6 (3.8)

NS

NS

NS

NS

NS

NS

(4)

ms

800

700

600

500

-28

Fig. 2a.

21 14

Day of Menstrual

Average duration of sleep spindle

There was no common tendency subjects. The average frequency was Iow abou£

l4 days before meRstrua£ioR, then increased and again decyeased about the first day of meRstruation. This change was significant

(p<O.e05) in all subjects in ANOVA.

Max-imum, minimum and F values for spindle

frequency ilt the subjects were MO :13.03,

13.36, 51.2, HN=12.9, 13.11, 53.75,

MI :13.09, 13.33, 41.68, YK= 12.81, 18.01, 12.32 and MT==12.97, 13.22, 35.92 (Fig. 2d).

4) Changes in the structure of the sleep slow

wave analyzed by means of the autoaRalysis

system.

Changes in the sleep slow wave which are as

important for the sleep EEG as the sleep

spiRdle were s£udied. The sleep slow wave was defined as O.5-1.5 Hz because waves in this frequency baltd most adequately reflect the change in the enti}"e sleep slow wave

Cycle

for the pattern

7

---・- m・・---・---

yes--mo

HN

MI

YK

MT

to change in these subjects.

out the night (Hamada. Personal

commucica-tion).

The structure of the slow wave iR this

analyzing system is the total number of slow waves, deRsity (number per minute), average amplitude and average frequency.

Figure 3 shows the density. There is no common pattern ofchaRge for the five sLibjects aRd there is no relationship to the menstrua} cycle. No other slow wave parameter is related to the menstrual cycle.

DIscussloN

It is widely recogRized that in most wornen the menstrual cycle is accompaRied by chaRges

in subjective sleep feelings. We studied

women'

s subjective evaluation of sleep by

(5)

pV

40

30

20

to

-28 -21 -14 -7

Day ef Menstrual Cycle

Fig. 2b. Average amplitude of sleep spindle

Although changes in amplitude are statistically considerable differences among subjects and the menstrual cycle.

Azumi's) Sleep Inventory5) and found that the subjective sleep feelings educed by means of

the inventory change with the menstrual

cycle}).

A look at the pattern of changes in the five sleep feelings shows that, generally, sleep feelings are worse in the second half (high

temperature,luteal phase) than iR the first half

(low temperature, follicular phase) of the

menstrual cycle. Based on the results ofearlier

studies, we attempted to determine if there

were polysomnographic changes during the

menstrual cycle. Some results of a pilot study

dealing with the same '£heme have already been reported6).

(I) Results of visual sleep stage scoriRg

ln the preseRt study, no significai}t changes

in sleep parameters be£ween the low and the

o

significant pattern of

7

-"--'"--)e--.-pt ・・・---・・"---・----・ -・---・- o-・----...---zCX--""M'

in three subjects, there change was not related

mo

nm

Ml

YK

MT

were to the

high temperature phases were found. In previeus studies by various researchers

on the menstrual cycle, sex hormones and

sleep, in which polysomnography was

em-ployed, the followiRg information was

obtained.

Ho reported that in humaR subjects before the menstrual period, although the amount of

slow wave sleep was reduced, other sleep

pavameters were Rot appreciably changed7).

HartmanB reported that the amouBt of REM

s}eep increased immediately before the

men-strual peyiod8)'9>. Lee compared the follicular

and luteal phases and reported that, although the period of REM sleep lateRcy was longer iR

the follicular phase than ilt the luteal phase,

theye was no chaRge in other sleep

(6)

Nurn!min

8

'Fig. 2c.

7

6

5

4

3

2

+ mo

---・----・--

be-- HN

----"---・--- Ml

+ YK

--

2t)r'-' MT 1

-28 -21 -14 -7 O 7

Day of Menstruai Cycle

Density (number per minute) of sleep spindle

In all subjects, the density increased after about 14th day of the menstrual cycle and began to decrease as the beginning of the menstrtial period approached. These change were statistically significant (p<O.O05) in all subjects.

change in sleep parameters during the men-strual cycleii). The resu}ts obtained in this study, according to Rechtschaffen and Kales criteria, support Kapen's report. Taking all of

these results together, it seems that evelt if sex

hormone or menstrual cycle related chaRges occur in the sleep structure, such changes are very small.

However, the reasen no c}ear polysomno-graphic changes during the menstrual cycle have been reported may be that researchers have depended solely on Rechtschaflbn and Kales criteria. Although the Rechtschaffen and Kales criteria offer many advantages, they define stages 3 and 4 by making a large 20% and 50% slow wave divisioit. For example,

according to those criteria, an epoch which has

20% slow waves and an epoch which has 49% slow waves are both defined as stage 3. This

definition is toe bread to use in distinguishing

sleep changes, especially NREM sleep changes,

in detail.

(2) Sleep spiRdle structure aRalyzecl with

autoallalyzer

In this study, by au£oanalysis with a persoital

computer, it was found that the average

frequency of the sleep spindle changes with

the menstrual cycle. Recently, a lot of fruitfu1

research has been doRe on changes in the

spindle and on the slow wave itselfi2)wwi4), however, there are few reports referring to

spindle frequegcy. Principe et al. reported that the spiRdle frequency ofa child is low aRCI that

of an elderly person is highi5). Using the autoaRalyzing method, especially with PSDA,

changes in the spiRdle structure, especially its

frequency, correspeRding to various body co

(7)

Hz

1 3,4 1 3.3 1 3.2 1 3.1 1 3.0 1 2,9 1 2,

8

---- mo

---

M-- HN

--・-de---- Ml

+ YK

--・---

A---- MT

M

Fig. 2d.

Day of Menstrual Cycle

Average frequency of sleep spindle

There was a clear pattern efchange in the sleep spindle frequency in five subjects. Frequency was low until 14th day of the iinenstrual cycle. After that, frequency increased and then decreased again about the beginning of menstruation. This change was statistically significant(p<O.O05) in all subjects.

Usui reported that the average frequency of the spindle ii3 delayed sleep phase syndreme

chaltged when various treatments were

triedi6).

It has been reperted that, even in a healthy person, spindle frequency chaRges as coAdi-tions chai}ge. Shirakawa reported differences in night sleep spindle structure after sleep deprivatioR and after a daytime nap. Accord-ing to his report, in nighttime recovery after sleep deprivation, the sleep spindle frequeRcy became lower, and that on a night after a daytime Rap became higher}2). In this present study also, the most characteristic change

accompanying the menstrual cycle was the

chaltge in the average frequency of the sleep

spindle.

From the yesults of £his study and

Shiraka-wa' s, it can be found tha£ the spindle frequency

becomes low in the low temperature phase as in night sleep after sleep deprivation, and it becomes high iR the high £emperature phase as

in night sleep after a daytime nap. IR our study

coBduc£ed with the sleep inventory, we found that women's sleep conditioR changes during

the mensti"ual cycle. For example, sleep ini£ia-tion is better and sleep is more sound at night

in the low temperature phase, whereas, sleep

initiation is worse and sleep is less sound ix the

high temperature phase. From the resu}ts of our study ofsubjective sleep feeling and those of the sleep spiRdle, it may be hypothesized that the sleep spiRdle frequeRcy is Iow when sleep propensi£y is high and the sleep

(8)

condi-64 Y. Ishizuka

num 1 min

16

Fig. 3.

14

12

10

8

6

+ mo

---

,e-- HN

--F--- Ml

+ YK

-'-=t)r-"-- MT 4

-28 -21 -14 -7 O 7

Day ef Menstural Cycle

Density of sleep slow wave

Densi£y (number per minute) of the slow wave which had a O.5-1.5 Hz frequeRcy and over 50 paV amplitude are shown in this figure. The sleep slow wave did notchange during the menstrual cycle in a manner comparable to the change in the frequency of the sleep spindle.

tion at night is good, but that it is high when sleep propensity is iow and the sleep condition

at night is bad.

The exac£ mechanism of the sleep spiRdle

appearance is not yet suMciently clear, but the

thalamic reticular nucleus is reported to form

the spindle or to modulate its frequencyi7)・i8).

To put it the other way around, it should be possible to guess the function of the thalamic reticular nucleus from the sleep spindle fre-quency.

The exact mechanisrn of the sleep spindle

modi.}lating effect on the central nervous

sys-tem (CNS) is stil} unknown, but sex hormones may play a role in this mechanism. OvariaR stereids are kRown to infiuence CNS function. Colvin reported that the amount of REM sleep

iR rats was decreased by estrogen

administrationi9). Ramirez reported that

in-travenous iajections of progesterone exert brief gelteralized anesthetic effects on EEG and hypothalamic unit firing rates in rats20).

Moreover, Nikiforova mentioRed that £he

longterm removal of sex hormone secretion iR rats causes a discrepancy betweeR the decrease in behavioral pattems and increased

excitabil-ity in CNS2i). Moreover it is knowR that

nuclear progesterone receptors exist in the hypothalmus and anterior hypephysis22). The spindle frequency chaltge noted in this s£udy may be derived from changes in the amounts of sex hormones associated with £he menstrual

cycle.

The sleep spindle is a very useful parameter

in studying sleep because ofthe reproducibility

of its appearance pattern. The autonomic

function is reported to change during the menstrual cycle23), but there are no detailed

(9)

reports ofchanges in the sleep EEG during the

menstrual cycle. It is very interesting that the

sleep spindle structure chaRges regularly dur-ing the menstrual cycle because the spindle might reflect brain function.

(3) Slow wave structure analyzed with the autoaRalyzer

The sleep slow wave did not change during the menstrual cycle in a manner comparable to the change in the sleep spindle frequency. Moreover, there are differences among

sub-jects and in the same subject in £he study night.

From the results of visual scoring, it was Rot possible to find a regular pattem ofchange in the slow wave sleep (iR stages 3 and 4) duriRg the menstrual cycle. In view of these results, and those of other researchers, it can be coRcluded that there are Ro changes iR slow wave sleep during the menstrual cycle. Until recently, sleep research has been based

on visua} scoring of the sleep stages. But now,

by means of a Bew auto-analyzing system

incorporating a personal computer, we caB easily do a frequency analysis ef the sleep

spindle. By this r}ethod, it was found

objective-ly that the known chaRges in subjective sleep feelings accompany the changes in the sleep spindle frequency. I£ is plaRned to further study other body phenomena which might be related to chaRges in the spindle frequeRcy,

and to clarify the relationship be£ween

subjec-tive sleep feeling and the sleep spindle.

ACKNOWLEDGEMENTS

I"he author is grateful to Pro£ Tetsuhiko

Kariya for his valuable commeRts on the

manuscript. The author also thanks Associate Pro£ Hitoshi Fukuzawa, Dr. Kazuo Azumi and Dr, Shuichiro Shirakawa for advice and

en-couragement, aRd Dr. Akira Usui, aRd Dr.

Kouichi Shiraishi for valuable assistance. [lrhis study was supported in part by Grant-in-Aid for Scientific Research No. 6S770812 aRd No. O17708l4 from the Ministry of Educa-tion of Japan.

REFERENCES

1) lshizuka Y, Usui A, Shiraishi S, et al. The Menstrual Cycle and the Subjective Evaluation of Sleep. Yamanashi Med J 1989; 4: 141-148.

2) dized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects.

Public Health Service, US 6overnment ing Office, Washington, D.C. 1968.

S) Shirakawa S, Azumi K, Smith J.R. Real Time Spindle Analyzer by Using Microcomputer. Jpn J EEG EMG }987; 15: 338-341. 4) Shirakawa S, Ishizuka Y, Azumi K. ment of Real Time Analyzing System of High Voltage Delta Waves by Using Microcomputer in Sleep. Jpn J EEG EMG 1989; 17: 37-44. 5) OguriM,ShirakawaS,AzumiK.Construction of Standard Rating Sca}e to Estimate Sleep

Profile. Seishin Igaku 1985; 27: 791-799. 6) Ishizuka Y, Usui A, Fukuzawa H, et al. strual Cycle and Frequency of Sleep Spindle.

Jpn J EEG EMG l990; 18: 489-445. 7) Ho A. Sex Hormones and Sleep of Women. Sleep Res 1972; 1: l84.

8) Hartmann E. Dreaming Sleep (The D-Stat.e) and The Menstrual Cycle. The Journal of Nervous and Mental Disease 1966; l43: 4O5-415.

9) Hartmann E. The Biology of Dreaming,

Charles C Thornas, Springfield, l967.

Ie) ature, and Mood State in Healthy Women at

Two Phases ofThe Menstrua} Cyc}e. Sleep Res

1987; 16: 624.

1l) Kapen S, Boyar R, Hellman L. Changes in the Sleep Stage Pattern during the Menstrual Cycle

of Normal Females. Sleep Res l972; 1: 186.

12) Shirakawa S, Ishizv{ka Y, Azumi K. Effects of

Total Sleep Deprivation and Nap on Spindle Function. Rinsko Nouha 1989; 31: 463-468. 13) Uchida S, Atsumi Y, Ishizuka Y, et al. The

Relatienship between Sleep Spindles and Sleep

Delta Waves. S}eep Res 1989; 18: 144.

I4) I<ubicki S, Scheuler W, Jobert M, et al. Der Einfiuss des Alters auf die Schlafspindel uncl

K-Komplexdichte. EEG EMG 1989; 20: 59-68.

15) Princip'eJC, SmithJR. Sleep Spindle teristics as a Function of Age. Sleep 1982; 5:

73-84.

16) Usui A, Iskizuka Y, Shiraishi K, et al. A Case With Delayed Sleep Phase Syndrome. Abstract

of IOth Congress of The ESRS 1990, 358. 17) Shosaku A, Kayama Y, Sumi£omo I, et al.

(10)

Analysis of Recurrent Inhibitory Circuit in Rat

Thalamus: Neurophysiology of the Thalamic

Reticular Nuc}eus, Progress in Neurobiology

1989; 32: 77-I02.

I8) Steriade M, McCarley RW. Brainstem Control

of Wakefulness and S}eep. Plenum Press, New

York, 1990; 2e8-217.

19) Colvin GB, Whitmoyer DI, Sawyer CH.

dian Sleep-Wakefulness Patterns in Rats after

Ovariectomy and Treatment with Estrogen. Exp. Neurol. I969; 25: 616-625.

20) RamirezVD,KomisarukBR,WhitmoyerDI,et

al, Effects of Hormones and Vaginal tion on the EEG and Hypothalarr}ic Units in Rats. Am. J. Physiol. 1967; 212: l376-1384.

21) Nikiforova AS, Patchev VK, Nikolov ND.

Ovarectomy- and Sex Hormone-induced

Changes in the Excjtability of the CNS; an Assessment by EEG Paroxysmal Activity and

Bel}aviour. Acta Physiologica et

ca Bulgarica l989; 15: 48-52.

22) Kato J, Onouchi "Ir. Nuclear Progesterone

Receptors and Characterization of Cytosol ceptors in the Rat H[ypethalamus and Anterior

Hypophysis. J Steroid Biochem 1979; ll: 845-854.

23) Little BC, Zahn TP. Changes in Mood 4nd Autonomic Functioning during the Menstrual

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