Modification of REM sleep behavior by REMs contingent auditory stimulation in man

Physiology&Behavior.Vol. 37, pp. 543-548. Copyright©Pergamon Press Ltd., 1986. Printed in the U.S.A.

0031-9384/86 $3.00 + .00

Modification of REM Sleep Behavior by REMs Contingent Auditory Stimulation in Man M. M O U Z E - A M A D Y , * t

P. S O C K E E L t

A N D P. L E C O N T E t

*Groupe d'Analyse Experimentale du Comportement (GRANEC), U.E.R. de Psychologie, Universite de Lille Ili BP 149, F-59653 Villeneuve d'Ascq, France tLaboratoire des Acquisitions Cognitives et Linguistiques (LABACOLIL), Universite de Lille Ill BP 149, F-59653 Villeneuve d'Ascq, France R e c e i v e d 6 D e c e m b e r 1985 MOUZE-AMADY, M., P. SOCKEEL AND P. LECONTE. Modificathm of REM sleep behavior by REMs contingent auditory stirnulation in man. PHYSIOL BEHAV 37(4) 543-548, 1986.--Following studies about supposed relationship between rapid eye movement sleep (REM sleep) and learning, a new approach, based on operant conditioning is introduced. We demonstrate that rapid eye movements (REMs) contingent auditory stimulation in man leads to some consistent (quantitative and qualitative) modifications of REM sleep behavior. Stimulating REMs in the frame of a continuous reinforcement schedule increases total REM sleep duration but decreases REMs density, and modifies hemispheric EEG symmetry. The contrasting effects of such sensory stimulations and results related to information processing hypothesis are discussed. REM sleep Learning Information Processing

Operant conditioning EEG Spectral analysis

REMs Density

Auditory stimulation

late that in man, some particular operant shaping contingencies (i.e., involving both reinforcement and punishment procedures [6]) can influence REM sleep.

IT has been reported that rapid eye movement sleep (REM sleep) may be involved in learning processes [10,12]. More precisely, some results show that acquisition of any complex skill leads to an increase of the subsequent REM sleep time of the subject (at least in the animal [10]), and especially just before learning completion [1]. In man, some qualitative aspects of REM sleep (phasic events) are related to learning performance. The oculomotor activity during this behavioral state seems to take a prominent part. The number of rapid eye movements (REMs) with interresponse times (IRTs) less than 1 second is correlated with skill success and/or mental efficiency [8, 9, 14, 20]. From such experimental data the information processing hypothesis (IPH) has arisen, which can be formulated as follows: one biological function of REM sleep, if not only one, is to ensure daily information processing. In a learning context, the temporal distribution of REMs may reflect the subject's ability to increase his order/noise ratio from environmental information input [15]. In order to expand the above-mentioned studies, about REM sleep and learning, we proposed a new approach based on the experimental analysis o f behavior [19] (i.e., operant conditioning methodology). Since, in the animal, considerable evidence indicates that acquisition of classical conditioned responses may occur during REM sleep [2] and, that REMs contingent activities (i.e., ponto-geniculo-occipital spikes) may be conditionable [5]. Consequently, we postu-

METHOD Four male students (23-24 years old with no history of neurological disease or brain damage) were polygraphically recorded (ECEM 2.3G, A6) for 3 consecutive nights: habituation, baseline and experimental night. Stick-on electrodes (ECEM E670) were placed at T3-01 and T4-02 (following the 10-20 standard system) with grounded frontal electrode. The time constant for the E E G signals was set at 1 sec with an upper cut off frequency at 50 c/sec. Eye movements were recorded from electrodes (ECEM Stabile 300) fixed above and below the right ocular epicanthus for the vertical EOG and on the left and right outer canthi for the horizontal EOG. EMG (surface electrodes below the chin) and E K G (ECEM E670 fixed with artificial skin OpSite Wound, Smith & Nephew 10x24 No. 4963) were also recorded for REM sleep detection. Sleep stages were classified according to standard criteria [17]. From the 8 recording channels, the horizontal EOG was selected for experimental control. This channel provided, via a REMs detector (INSERM, Semi Lyon, TO30), a digital signal which generated, during the third night, an audio feedback (40 msec duration) from a white noise generator (Motorola, MM 5837). The auditory stimulation was fed

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O P E R A N T M O D I F I C A T I O N O F REM S L E E P

545

TABLE 1 QUANTITATIVE RESULTS: COMPARISONSBETWEEN BASELINEAND EXPERIMENTALDATAIN 4 SUBJECTS Subject 1

Number of REM periods Total REM sleep duration (min) [1] Mean REM period duration (min) REM sleep/ Total sleep (%) Total number of REMs [2] Total Density per min

Subject 2

Subject 3

Subject 4

Base.

Exp.

Base.

Exp.

Base.

Exp.

Base.

Exp.

4

5

4

5

4

6

5

6

118.46

185.53

95.00

145.33

139.20

162.10

29.41

37.03

24.15

29.07

35.23

27.01

30.08

35.33

29.62

42.65

24.24

34.60

25.92

33.01

28.21

42.49

1623

358

525

187

630

531

988

685

5.53

1.29

4.53

6.66

3.23

13.70

1.93

3.28

148.40 212.00

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through mini headphones (Kenwood KH-M5, 7 0 - 9 2 dB range intensity). This channel also allowed computer (Commodore CBM 8000) interrupts for REMs counting and real time burst detection (Fig. 1). F o r subject 4, right and left hemisphere EEG signals were digitized on line during the REM sleep periods. The A/D converter, built around an AD 7574 chip (Analog Devices) and controlled by a microprocessor, was activated by the experimenter. The procedure used for F F T computation [3] required a 10.24 sec conversion period at a 102.4 c/sec sampling rate. To provide for removal of epochs containing artifacts (generally muscle discharges), 6 consecutive E E G samples (for each left and right montage) were recorded without any gap. After disk storage completion the procedure was reactivated during the whole REM period.

Spectral Analysis of the EEG Spectral analyses were performed on E E G data (within the REM sleep periods) recorded during the baseline and the experimental night in subject 4 as an exploratory study. Prior to any computation, a collaborator, blind to the experimental conditions, reviewed on a CRT terminal each of the E E G records for artifact identification. The epochs containing more than 5% artifacts were deleted. The remaining samples were filtered with a recursive digital filter simulating a Tchebycheff bandpass filter (1.1-35 c/sec) with a 36 dB/octave rolloff. The relative power spectra (Fig. 2) were calculated (BFM 186 computer, YE DATA) by the F F T method on 1024 channels (Nyquist frequency: 51.2 c/sec and resolution frequency: 0.1 c/sec. To extract relevant information, only the first 300 channels (up to 30 c/sec) were taken into account for further investigation. In order to track the amplitude variations of specific frequencies, the relative power of the 300 F F T channels were packed into 15 bands of 2 c/sec width, providing facilities for statistical analysis on the 320 computed spectra (about 20 rain of signal in each night condition).

RESULTS

Quantitative Aspects As shown in Table 1, REMs contingent auditory stimulation leads to some consistent modifications in REM sleep behavior. We observed that the total REM sleep duration was increased to a great extent (16.45%-56.62%). In all subjects the number of REM sleep periods was increased: more precisely, subjects 1, 2 and 4 showed both an increase in number of REM sleep epochs (by one unit) and in mean REM sleep period duration, whereas subject 3 showed a decrease in mean REM sleep phase duration but an increase of 2 REM sleep phases. Moreover, we noticed a drop in REMs density ( - 15.71%--77.94%) for each subject. This fall seemed to be correlated with the REM sleep ratio increase (Fig. 3): the more important the increase in the REM sleep ratio, the greater the decrease in the REMs density.

Qualitative Aspects The main activity was found in the first 3 bands (0 to 6 c/sec) but no significant result stood out from the different sources of variation (REM sleep stages, baseline/experimental nights) except an interhemispheric asymmetry as reported in Fig. 4. Considering the statistically significant comparisons (Student's t-test), the most important finding is an absence of lateralized difference during baseline night with a disruption of this interhemispheric balance on the experimental night for REM periods 2 to 4. This electrical activation of the left derivation was most evident after later analysis of variance on each different 2 c/sec band (only the first 4 REM sleep stages of the 2 nights were included for the A N O V A design). Strong lateralization tendencies were observed in the 8--10 c/sec channel (corresponding to alpha 1 band), F(1,300)=8.34, p<0.01, with a

546

MOUZE-AMADY, S O C K E E L AND L E C O N T E

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FIG. 3. Comparisons between REM sleep and REMs activity modifications. Open columns: % of REM sleep increase; lined columns: % of REMs activity impairment.

significant interaction between night condition (baseline versus experimental) and right/left derivations, F(1,300)=5.71, p<0.05, and between these 2 sources of variation and REM sleep period, F(3,300)=2.76, p<0.05. Figure 5 shows the mean differences in this band through REM sleep stages: the left electrical response occurs in the second REM epoch (middle of the experimental night), F(1,300) =21.22, p<0.01, with a further tendency to fade out. DISCUSSION

Quantitative Modifications On the basis of our experimental data it can be pointed out that REMs contingent auditory stimulation increases REM sleep. Behaviorally speaking, the auditory stimulus, on a continuous reinforcement schedule (REMs contingent), is a positive reinforcer of tonic REM sleep behavior. We simi-

larly note that the stimulation is a positive punishment (i.e., contingencies which, added (positive) to a situation, decrease the probability of the response [6]) for 100/zV horizontal REMs. Our results are consistent with Drucker-Colin's findings [5] in the animal, in which it was suggested that a sensory signal could act as a REM sleep reinforcer. Nevertheless, in order to explain the contrasting effects of the stimulation it may be necessary to examine the fine grain of REMs behavior as indicated by a detailed interresponse times (IRTs) analysis, since the "fine structure of operant behavior during transition s t a t e s . . , may specify the precise control of how discriminations develop" [21]. REMs IRTs analysis are in progress in our laboratory. Furthermore, one can expect, from such analysis, to find an operational definition of REMs bursts. From a theoretical point of view, as previously related

O P E R A N T M O D I F I C A T I O N O F REM S L E E P

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FIG. 4. Distribution of REM sleep relative EEG power asymmetry (left minus right hemisphere) in baseline night and experimental night. Darkened columns show the significance differences at t-test for p<0.01.

[11], REMs activity can be considered as an autonomous behavior. Thus the contrasting effects of the auditory stimulus are not inconsistent. REMs activity and REM sleep are two classes of responses. In this case, the question becomes: first, is there some stimulus (possibly a task, see below) which is punishing (or without perceptible effects) for REM sleep behavior and reinforcing for REMs activity?; second, what is the functional relationship between REMs density and REM sleep rate when stimulation is response-dependent (i.e., REMs contingent)? Experimental designs have already been devised in order to try and solve this question.

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Qualitative Modifications Following Goldstein's first results [7], a number of studies examined dominance of homologous brain areas or interhemispheric asymmetry relationship during sleep, assuming that electrophysiological changes were related to behavioral states. With respect to the integrated E E G amplitude from left and right hemisphere or the electrical power in a specific band of frequencies, it is generally agreed that a higher amplitude indicates less hemispheric involvement [16]. Accordingly, it was reported that power asymmetry during sleep was related to handedness [4,18]: right handed subjects showed a relative right activation in REM sleep, especially in the alpha b a n d - - c o n s i s t e n t with mediation of visuo spatial

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2

3

4

FIG. 5. REM sleep relative EEG asymmetry (% left minus right hemisphere) in the 8-10 c/sec band. Calculations were performed for each period over the first 4 REM sleep epochs during baseline (dotted line) and experimental night (full line).

548

MOUZE-AMADY, SOCKEEL AND L E C O N T E

processes--while the phenomenon was reversed in the left handed [ 13]. The baseline night of subject 4 (right handed) failed to show any hemispheric dominance, except a slight left activation in period 2 and 3. In contrast, the significant increase of relative right activity on the experimental night may be related to the auditory stimulation conditions (primarily perceptual processes). With allowance for necessary replication, the quantitative data of this study (number of REM sleep periods, REM sleep duration) and the subjects' report on awakening the following morning are consistent with the assumption that such a reinforcement procedure may improve sleep quality. In conclusion, our results suggest the existence of a relationship between tonic and phasic aspects of REM sleep, since a decrease of REMs density is linked with an increase of REM sleep duration. With reference to the IPH paradigm, we reported that, in man, learning a calculating skill in Basic

language involved a significant increase of REMs density without modification in the REM sleep duration [20], whereas learning Morse language involved an increase of REM sleep periods without modification of REMs activity (Mandai ~,t al., in preparation). Such effects could be due to the nature of the tasks: visuo-semantic versus auditory skill, but in both situations, learning involved an increase in the absolute number of phasic events: in the first case by lengthening the period in which phasic events occur, in the second case by increasing frequency of phasic events, which is a hypothetical expression of cerebral activation necessary for information processing. The results described in this paper show that operant methodology can make the relationship between REM sleep and REMs characteristics clearer. Moreover, it justifies the possibility of some experimental control of information processing through the instrumentality of phasic and/or tonic REM sleep components conditioning.

REFERENCES

1. Bloch, V., E. Hennevin and P. Leconte. Les etapes de l'acquisition et le traitement hypnique de l'information. In: Psychologie Experimentale et Comparee. hommage a P. Fraisse. Paris: P.U.F., 1977. 2. Bloch, V. and C. Maho. Acquisition of classical conditioning during REM sleep in rats, Communication of the 4th International Congress of Sleep Research, APSS, Bologna, 1983. 3. Cooley, J. W. and J. Tukey. An algorithm for machine calculation of complex Fourier series. Math Computation 19: 297-301, 1965. 4. Doyle, J. C., R. E. Ornstein and D. Galin. Lateral specialization of cognitive mode: EEG frequency analysis. Psyehophysiology 11: 567-578, 1974. 5. Drucker-Colin, R., J. Bernal Pedraza, F. Fernandez Cancino and A. R. Morrison. Increasing PGO spike density by auditory stimulation increases the duration and decreases the latency of rapid eye movement (REM) sleep. Brain Res 278: 308-312, 1983. 6. Freixa I Baque, E. Une mise au point de quelques concepts et termes employes dans le domaine du conditionnementoperant. Annee Psychol 81: 123-129, 1981. 7. Goldstein, L., N. W. Stoltzfus and J. F. Gardocki. Changes in interhemispheric amplitude relationships in the EEG during sleep. Physiol Behav 8:811-815, 1972. 8. Grubar, J. C. Sleep and mental deficiency. Rev Eleetroeneephalogr Neurophysiol 13: 107-114, 1983. 9. Grubar, J. C. Sleep and mental efficiency. In: The Psychology of Gifted Children, edited by J, Freeman. New York: J. Wiley and Sons, Ltd, 1985, pp. 141-157. 10. Hennevin, E. and P, Leconte. Etude des relations entre le sommeil paradoxal et les processus d'acquisition. Physiol Behav 18: 307-319, 1977. 11. Hoffmann, H., H. Wauters, E. Pauwels, G. Buytaert, F. Uyttenbroeck and O. Petre-Quadens. Sleep and pituitary hormones. A comparative study between premenopause and menopause, Waking Sleeping 2: 157-167, 1978.

12. McGrath, M. J. and D. B. Cohen. REM sleep facilitation of adaptative waking behavior: a review of the literature. Psyehol Ball 85: 24-57, 1978. 13. Murri, L., A. Stefanini, E. Bonanni, G. Cei. C. Navona and S. Denoth. Hemispheric EEG differences during REM sleep in dextrals and sinistrals. Res Comman Psy~.hol Psyehiatr Beh~' 9: 109-120, 1984, 14. Petre Quadens, O. and C. De Lee. Eye movements during sleep: common criterion of learning capacities and endocrine activity. Dev Med Child Neurol 12: 730-740, 1970. 15. Petre Quadens, O. Logic and ontogenesis of some sleep patterns. Totus Homo 8: 60-72, 1978. 16. Pivik, R. T., F. Bylsma, K. Busby and S. Sawyer. lnterhemispheric EEG changes: Relationship to sleep and dreams in gifted adolescents. Psychiatr Univ Ottawa 7: 56--76, 1982. 17. Rechtschaffen, A. and A. Kales. (Eds). A Manual of Standardized Terminology, Teehniqaes and S~'oring System for Sleep Stages of Human Subjects. Washington, DC: United States Government Printing Office, 1%8. (National Institute of Health Publication No. 204). 18. Rosekind, M. R,, T. J. Coates and V. P. Zarcone. Lateral dominance during wakefulness, NREM stage 2 sleep and REM sleep. Sleep Res 8: 36, 1979. 19. Skinner. B. F. Some contributions of an experimental analysis of behavior to psychology as a whole. Am Psyehol 8: 69-78, 1953. 20. Spreux, F., C. Lambert, B. Chevalier, H. Meriaux. E. Freixa 1 Baque, J. C. Grubar, A. Lancry and P. Leconte. Modifications des caracteristiques du sommeil paradoxal consecutif a un apprentissage chez l'Homme. Cah Psychol Cogn 2: 327-334, 1982. 21. Weiss, B. The fine structure of operant behavior during transition states. In: The Theory of Reinfi~rcement Seheduh, s. edited by W. N. Schoenfeld. New York: Appleton-Century Crofts, The Century Psychology Series, 277-31 I, 1970.