Theta spindles in human R.E.M. sleep

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Theta spindles in human R.E.M. sleep. P. T. S. PUTKONENand E. ELOMAA. Institute of Physiology, University of Helsinki Siltavuorenpenger, 20, Helsinki 17, Finland.

INTRODUCTION. Classic descriptions of R . E . M . stage (e. g. DEMENT a n d KLEITMAN, 1957 ; JOUVET et al., 1960) m e n t i o n occasional trains o f low, regular 5-7 c/sec waves against t h e low voltage m i x e d frequency b a c k g r o u n d , a n d a small t h e t a peak is evident in t h e E.E.G. spectra of R . E . M . in s o m e subjects (JOHNSON et al., 1969). T h e p r e s e n t n o t e illustrates a n adult subject s h o w i n g s p i n d l e f o r m b u t t s of high r h y t h m i c theta as a salient feature o f his R . E . M . periods. A s these theta spindles s t o o d out clearly against the lower E.E.G. b a c k g r o u n d it was n o t e d that they were regularly m o r e f r e q u e n t in the evening t h a n in t h e m o r n i n g R . E . M . periods. Because of this u n e v e n distribution we feel that they m a y have interest b e y o n d a m e r e E.E.G. curiosity as an indicator o f s o m e generally m o r e subtle E.E.G. differencies between successive R . E . M . periods o f a n i g h t ' s sleep.

Subject and methods The phenomenon was noted in a healthy 29 years old male physician who volunteered as a subject in a sleep study unrelated to the present report. A routine E.E.G. examination in the awake state showed 9-1 0 c/see alpha and contained no abnormalities. Disc electrodes placed according to the manual of RECrITSCffAF~EN and KALES (1968) were used tbr sleep recording. As a rule only one cortical lead : C4-A1 (International 10-20 system) was used. F4 and P4 were added once (Fig. 1). Whole night records of undisturbed sleep were obtained using a time constant of 0.1-0.3 sec and a paper speed of 15 ram/see. E.E.Gs from two nights were also taken on F M tape. Representative I0 sec samples, chosen from the tape, were digitized bya ~-Linc computer for calculation (see PUTKONEN et al., 1968) of their autocorrelograms and frequency spectra (Figs. 2 and 3). RESULTS. Bursts o f r h y t h m i c theta in R . E . M . sleep were seen in altogether seven nights recorded d u r i n g 15 m o n t h s . W e restrict this report, however, to three <>laboratory nights o f n o r m a l sleep which contained a total of 78 theta bursts. T h e bursts typically h a d a s p i n d l e f o r m envelope, reached an a m p l i t u d e of ca 75-100 s V , a n d were m o s t p r o m i n e n t in t h e frontal area (fig. 1). T h e i r m e a n lenght (2_ S.D.) was 4.8 ~ 2.3 sec. Spectral analysis o f 10 sec E.E.G. s a m p l e s c o n t a i n i n g t h e t a b u r s t s g a v e a consistent frequency peak at 7 c/sec with a h a r m o n i c peak at 3.5 c/sec (fig. 2 a n d 3 a). Occasionally t h e 3.5 c/sec, activity could d o m i n a t e a n d give t h e m a <> appearance. E.E.G. samples o f R . E . M . disregarding the bursts gave spectra o f m i x e d delta a n d theta with d o m i n a n c e in the slowest b a n d s , a n d n o distinct peaks (fig. 3 b). T h e theta bursts were practically c o n f i n e d to the R . E . M . stage with only five o f the 78 bursts seen in stage 2 usually heralding a c h a n g e to R . E . M . H i g h r h y t h m i c theta was n e v e r seen in the a w a k e stage in routine clinical E.E.G., n o r d u r i n g m e n t a l tasks. In sleep the theta bursts a p p e a r e d m a i n l y in the first two R . E . M . periods a n d tended to disappear towards m o r n i n g . F o r the three nights the average theta percentages (== 100 × s u m m e d ® burst time/lenght of R . E . M . period) for the first,

Tirds ?t part : P. T. S. PI3TKONEN(~1.l'adresse ci-dessus).

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second, third and fourth R.E.M. periods were 6 p. 100, 3 p. 100, 1 p. 100 and 0 p. 100 respectively. For comparison, an assessment of eye motility according to ASERINSKY'S (1971) <~method (I ° = 8 sec.) gave eye movement percentages of 7 p. 100, 13 p. 100, 20 p. 100 and 13 p. 100 for R.E.M. periods 1, 2, 3, and 4. Inside the periods the theta burts were not associated with eye movements. Contrary to what has been shown for ~< saw tooth >> waves (C. BERGER et al., 1962) not a single cluster of eye movements occured within the 5 sec periods following the beginning of theta bursts.

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FIG. 3. - - (A) Two frequency spectra of theta bursts in R.E.M. showing maximal range of variation between the proportions of the 7 and 3.5 c/see peaks. (B) Two spectra of R.E.M. <) activity from the same (C4-A1) lead. Spectral intensities plotted in arbitrary units.

DISCUSSION. Rhythmic theta has not been emphasized in connection with human stage R.E.M. In this case high spindlelike bursts of 7 c/sec waves with varying proportions of 3.5 c/sec harmonic form a very distinct transient pattern of R.E.M. stage. They are probably not a variant of the ~ saw tooth)) waves, (JoUVET et al., 1960) in spite of occasional resemblance, since the latter appear in conjunction with eye movements in both humans (BERBER et al., 1962) and the chimpanzee (Fm~EMON et al., 1970) whereas this was not true for the theta spindles. On the other hand they may be related to theta trains described by DEMENT and KLEI:rMAN (1957). According to them, there were among the irregular E.E.G. pattern of R.E.M. ~ also many bursts or trains of regular 7-10 per sec. waves in the occipital leads, and 18-25 or 5-7 per sec. waves in the frontals. )) They also state that : ~ These synchronous

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patterns were somewhat m o r e prominent in the intervals between cluster o f eye movements... >>In Fig. 2 o f the cited paper, subject B.D. shows a distinct alpha (ca. 8 c/sec) burst with clear occipital dominance, which together with a higher frequency distinguishes it f r o m our frontal theta. A n o t h e r example f r o m the same subject, however, shows a less distinct ca. 6 c/sec frontal burst and a second subject (H.J.) displays a predominantly frontal, ca. 7 c/sec spindle resembling the present bursts in all but a smaller amplitude (barely 50 b~V). This leads us to presume that the high rhythmic theta in our subject may represent an u n c o m m o n l y ample and distinct variant o f a more general, but usually elusive feature in the E.E.G. o f R.E.M. The theta bursts were m o r e a b u n d a n t in the R.E.M. periods o f the first half o f the night virtually disappearing towards morning. In this they were diagonally opposed to eye movements (e.g. ASERINSKY, 1971) << saw t o o t h >> waves (FREEMON et al., 1970), and also erections (JOvANOWC, 1971), which are all intensified towards morning sleep. Thus they add an interesting E.E.G. aspect to the asymmetry o f overnight sleep. The fact that our subject never produced similar bursts of rhythmic theta in stage 1, when failing asleep, seems to set the p h e n o m e n o n apart from the hypnagocic theta, prevalent in children (e.g. MAULSBY, 1971). The association of stage R.E.M. to dreaming makes it tempting to speculate on possible correlations o f the R.E.M. theta to trains o f theta reported in some awake subjects in conjunction with (a) emotional reactions, (b) various mental tasks, and (c) visual imagery (e.g. WALTER, 1950 ; MONOYCASTLE, 1957 ; KASAMATSUand HIRAI, 1969 ; MAULSBY, 1971 and ISHIHARA and YOSHlt, 1972) althrough no bursts o f rhythmic theta were seen in our subject during wakefulness. BIBLIOGRAPHIE 1. ASERINSKY(E.). Rapid eye movement density and pattern in the sleep of normal young adults. Psychophysiol., 1971, 8, 361-375. 2. BERGER (R. J.), OLLEV (P.) and OSWALD (I.). The E.E.G., eye-movements and dreams of the blind. Quart. J. Exp. Psychol., 1962, 14, 183-186. 3. DEMENT (W.) and KLEIT~AN (N.). Cyclic variations in E.E.G. during sleep and their relation to eye movements, body motility, and dreaming. Electroenceph. elin. NeurophysioL, 1957, 9, 673-690. 4. FREEMON(F. R.), McNEw (J. J.) and ADEY (W. R.). Sleep of unrestrained chimpanzee : Differences between first and last rapid eye movement periods. Folia primat., 1970, 13, 144-149. 5. ISmHARA (T.) and Yosrm (N.). Multivariate analytic study of E.E.G. and mental activity in juvenile delinquents. Eleetroenceph. clin. Neurophysiol., 1972, 33, 71-80. 6. JOHNSON(L.), LUmN (A.), NAtTOH (P.), NUTE (C.) and AUSTIN (M.). Spectral analysis of the E.E.G. of dominant and non-dominant alpha subjects during waking and sleeping. Eleetroeneeph. eBn. Neurophysiol., 1969, 26, 361-370. 7. JotrWT (M.), MICHEL (F.) et MotrNmR (D.). Analyse 61ectroenc6phalographique compar6e du sommeil physiologique chez le chat et chez l'homme. Rev. neuroL, 1960, 103, 189-205. 8. JOVANOV~C(U. J.). Erektionen im Schlaf und vegetative Funktionen. J. neurovise. ReL, 1971, 32, 200216. 9. KASAMATStr(A.) and HmAt (T.). An electroencephalographic study on the Zen meditation (Zazen). In : C. T. TART (Ed.). Altered states of conciousness. John Wiley, edit., N. Y., 1969, 481-510 (cited from MAULSBY, 1971). 10. MAULSBY(R. L.). An illustration of emotionally evoked theta rhythm in infancy : Hedonie hypersynchrony. Electroenceph. clin. Neurophysiol., 1971, 31, 157-165. 11. MUNDY-CASTLE (A. C.). The electroencephalogram and mental activity. Electroenceph. clin. Neurophysiol., 1957, 9, 643-655. 12. PUTKONEN(P. T. S.), SARA$AS(I-I. S. S.) and STENBERG(D.). Computer analysis of hippocampal rhythm in hypothermic rabbits. Ann. Meat. exp. Fenn., 1968, 46, 552-556. 13. RECHTSCHAFFEN(A.) and KALES (A.) (Eds)./1 manual o f standardized terminology, techniques, and scoring system for sleep stages o f human subjects. N.I.H. Publication N ° 204, U.S. Government Printing Office, Washington D. C., 1968, 62 p. 14. WALTER (W. G.). The twenty-fourth Maudsley lecture : The functions o f the electrical rhythms in the brain. J. ment. Sci., 1950, 96, 1-31