H-Reflex Suppression and Autonomic Activation During Lucid REM Sleep: A Case Study

Transcription

1 Sleep 12(4): , Raven Press, Ltd., New York 1989 Association of Professional Sleep Societies Short Communication H-Reflex Suppression and Autonomic Activation During Lucid REM Sleep: A Case Study * Andrew Brylowski, Lynne Levitan, and Stephen LaBerge *University of Texas Medical School at Houston, Houston, Texas, and Sleep Research Center, Stanford University School of Medicine, Stanford, California, U.S.A. Summary: A single subject, a proficient lucid dreamer experienced with signaling the onset of lucidity (reflective consciousness of dreaming) by means of voluntary eye movements, spent 4 nonconsecutive nights in the sleep laboratory. The subject reported becoming lucid and signaling in 8 of the 18 rapid-eye movement (REM) periods recorded. Ten lucid dream reports were verified by polygraphic examination of signals, providing a total of 12.5 min of signalverified lucid REM. H-Reflex amplitude was recorded every 5 s, along with continuous recording of electroencephalogram, electrooculogram, electromyogram, electrocardiogram, finger pulse, and respiration. Significant findings included greater mean H-reflex suppression during lucid REM sleep than during nonlucid REM and correlations of H-reflex suppression with increased eye movement density, heart rate, and respiration rate. These results support previous studies reporting that lucid REM is not, as might be supposed, a state closer to awakening than ordinary, or nonlucid, REM; rather, lucid dreaming occurs during unequivocal REM sleep and is characteristically associated with phasic REM activation. Key Words: H-Reflex-Lucid REM sleep. Electrophysiological studies have shown that "lucid" dreams, in which persons are explicitly aware that they are dreaming while continuing to dream, occur almost exclusively in rapid-eye-movement (REM) sleep (1). Further investigations (2,3) have indicated that lucid REM sleep is characterized by higher levels of phasic activity and autonomic activation than ordinary REM sleep, and therefore that it is likely that lucidity occurs during periods of relatively great cortical activation. Contrary to some earlier suggestions that lucid dreaming might be the result of microawakenings, brief intrusions of waking consciousness, in REM periods (4), the findings that lucidity is Accepted for publication September Address correspondence and reprint requests to Dr. A. Brylowski at Department of Psychiatry, Southwestern Medical School at Dallas, 5323 Harry Hines Blvd., Dallas, TX , U.S.A. 374

2 H-REFLEX SUPPRESSION IN LUCID REM 375 associated with more intense, activated REM sleep suggest rather that lucid REM is a deep sleep state and not nearer to waking than ordinary REM sleep. The primary goal of this experiment was to investigate the status of H-reflex suppression in lucid dreams. Given that both human (5,6) and feline (7,8) studies have demonstrated tonic reflex inhibition during phasic REM and that lucidity is associated with phasically active REM, it was predicted that the H-reflex during lucid REM would be at least as suppressed as it is in ordinary REM. In the H-reflex analysis, the polygraph records were divided into 5-s epochs instead of the standard 30-s epochs (9), enabling correspondingly finer resolution of the state changes during REM and especially lucid REM sleep. It was possible to identify microawakenings and transitions to non-rem (NREM) sleep if any occurred during the periods of lucidity. METHODS The subject was a 25-year-old medical student, an experienced lucid dreamer who was familiar with the method of signaling from lucid dreams by means of eye movements verifiable on the polygraph record (1). His sleep was normal during an all-night polysomnogram without continuous H-reflex monitoring. On 4 nonconsecutive nights his H-reflex was measured as he slept with the intention to recognize when he was dreaming and to signal the onset of lucidity. The experimental protocol called for the subject to signal the onset of lucidity with two pairs of extreme left-right eye movements and to signal awakening with four pairs of left-right eye movements. The subject wrote reports of mental activity after each spontaneous awakening, including the times of awakening. Following previously described methodology (I), reports were scored as signal-verified lucid dreams if (a) the subject reported that he had become lucid and made the eye movement signals and (b) the corresponding section of the polygraph record showed the reported signals. A Grass model 8-18D was used to record several channels of electroencephalogram, induding the standard central positions used for sleep scoring, vertical and horizontal electrooculogram, electrocardiogram, nasal airflow, finger pulse, and H-reflex amplitude. Standard procedures for measuring H-reflex were used, modified for continuous measurement (10,11). The subject's knee was immobilized in a knee immobilizer set at 100 flexion and a O.I-ms 50-V stimulus was delivered to the right posterior tibial nerve every 5 s as the contraction of the soleus muscle was monitored. A TECA model TE42 electromyogram (EMG) machine provided the electrical stimulus and amplified the EMG signal, which was sent to the J5 external input on the Grass polygraph. The polygraph records were scored according to the standard criteria (9). The REM periods, including the 30 s pre and post REM, were subdivided into 5-s epochs, one epoch for each H-reflex sample. These 5-s epochs were again scored for sleep stages according to the standard criteria modified for 5-s epochs. An epoch was scored as Stage 2 if no change in stage had occurred between K-complexes or sleep spindles or if a K-complex or sleep spindle was present anywhere in the epoch. Also, an epoch was scored as lucid REM only if it contained an eye movement signal or lay between epochs containing signals corresponding with the subject's written report (see Fig. 1). In addition to sleep staging, several other physiological measures were collected and analyzed in 5-s epochs. These were H-reflex amplitude (millimeters of pen deflection), eye movement density (number of eye movements per epoch), heart rate (beats per

3 376 A. BR YLOWSKI ET AL. C4 A2 ~~I~ I V."""V~"'Ii.rl.~... r'~<'f\"\a~ Cz A2 ~I~~~l~~'\i'" YJ!},,j~NJtA,,,,\~f,MwJ(I!~... ~/r'"h\f\. T3 A1,~ tv~/' ~,~----~ T4 A2 ~V\f''''----V~t 01 A1 02 A2 LOC A1 ROC A2 F. Pulse EMG EKG H Reflex Resp \ \ \ ~ A. Awake B. REM Sleep ---==-----,150!l V 5 Sec FIG. 1. A: Awake, eyes closed. Two sets of eye movement signals are shown. B: REM sleep. Two sets of eye movement signals are shown, with the onset of a lucid dream at the first (arrow). Note the indications of autonomic activation [skin potential artifact in the electroencephalogram and electrocardiogram (EKG) chan nels and finger pulse amplitude suppression] and the profound H-reflex suppression accompanying lucidity. epoch converted for analysis to beats per minute), and respiration interval (measured for the breath cycle occupying >50% of the 5-s epoch and converted for analysis to breaths per minute). RESULTS Eighteen REM periods were recorded; eight included portions of lucid REM with a total of 10 lucid dreams. A total of 150 epochs (12.5 min) of lucid REM were collected across the 4 recording nights out of 2,470 REM epochs (206 min). The number of epochs oflucid REM for nights 1-4 was 18 (1.5 min), 18 (1.5 min), 48 (4 min), and 66 (5.5 min), respectively. The percentage of total sleep time spent in REM from nights 1 through 4 was 5.4% (19 min/349.5 min), 11.1% (60 min/538.5 min), 18.4% (64 min/348 min), and 29.4% (63 min/214.5 min), respectively. The increasing percentages of REM are presumably due to the subject adapting to sleeping under the difficult experimental conditions. Only the epochs within REM periods actually scored as REM were analyzed. None of the portions of lucid REM were found to contain any microawakenings or transitions to NREM. The mean H-reflex amplitude was determined for the nonlucid epochs and lucid epochs of each REM period that included lucid REM. In all eight cases, the mean H-reflex amplitude for lucid REM was lower than that for nonlucid REM (binomial test,

4 H-REFLEX SUPPRESSION IN LUCID REM 377 p = 0.(04). A one-tailed paired t test of the REM period means of lucid REM versus nonlucid also revealed lucid REM H-reflex amplitude to be significantly lower than nonlucid (t(7) = 4.43, p < 0.005). As mentioned above, previous studies have shown that the initiation Of lucidity in REM sleep is associated with autonomic activation (2,3). To examine the relationship between the onset of lucidity and H-reflex suppression, the mean values of H-reflex amplitude for the 30 s preceding and the 30 s following lucidity initiation were compared with the REM period median H-reflex amplitude. For both pre- and postlucidity periods, 8 of 10 mean amplitudes were lower than the all-rem period median amplitudes (binomial test, p = 0.05). The same type of comparison was performed on eye movement density in the 30 s pre- and postlucidity initiation. For all 10 lucid dreams, the eye movement density means were higher just before and after lucidity onset than the all-rem period medians (binomial test, p = 0.001), bearing 'Out the earlier findings on this measure of autonomic arousal. Direct comparisons of the relationship between H-reflex suppression and other autonomic variables were done with Spearman rank correlations of H-reflex amplitude with eye movement density, respiration rate, and heart rate. These tests showed highly significant (p < 0.001) negative correlations between H-reflex amplitude and all other physiological variables when the values from nights 1-4 were pooled. For the individual nights, 11 of 12 coefficients showed significant correlations (p < 0.05) (see Table O. DISCUSSION The results of the above comparisons of H-reflex amplitude during lucid and nonlucid REM sleep clearly show not only that H-reflex is suppressed during REM lucid dreams, as it is in ordinary REM sleep, but that it tends to be more suppressed during lucid than nonlucid REM. Increased H-reflex suppression was also strongly associated with phasic REM activity and autonomic activation, two factors that previous studies (2,3) have shown to also be associated with lucid REM sleep. The findings presented here demonstrate that lucid dreaming occurs during unambiguous REM sleep, without microawakenings or other arousals, and also that lucid REM sleep is associated with relatively high phasic activity, autonomic activation, and TABLE 1. Correlations of H-reflex amplitude with eye movement density, heart rate, and respiration rate for the 4 nights individually and pooled using Spearman's correlation coefficient H-Reflex amplitude with Eye movement density Heart rate Respiration rate Night 1 Night 2 Night 3 Night 4 All nights pooled " (n = 192) a (n = 981) a (n = 1,057) a (n = 970) " (n = 3,200) (n = 192) -O.3508 a (n = 980) -O.0698 b (n = I,OS9) a (n = 970) -O.3198 a (n = 3,201) -0.IS20 b (n = 191) S Q (n = 980) Q (n = I,OS6) -O.l164 Q (n == 962) " (n = 3,189) Q P < b P < O.OS.

5 378 A. BR YLOWSKI ET AL. deep reflex suppression. By showing that the H-reflex is even more suppressed during lucid REM than nonlucid REM, these analyses suggest that lucid REM is not, as might be supposed, a state closer to awakening than ordinary, or nonlucid REM. Additionally, a direct relationship is suggested between the depth of H-reflex suppression and increased phasic activation in REM sleep. Further research is indicated to confirm these findings with more subjects and to investigate in more detail the relationship between various modes of physiological activation, tonic reflex suppression, and the mental activity of the dreamer. Acknowledgment: The support of The Institute of Human Development is gratefully acknowledged. REFERENCES 1. LaBerge SP, Nagel LE, Dement WC, Zarcone VP. Lucid dreaming verified by volitional communication during REM sleep. Percept Mot Skills 1981 ;52: LaBerge SP, Nagel LE, Taylor WB, Dement WC, Zarcone VP. Psychophysiological correlates of the initiation of lucid dreaming. Sleep Res 1981 ;10: LaBerge S, Levitan L, Dement WC. Lucid dreaming: physiological correlates of consciousness during REM sleep. J Mind Behav 1986;7: Schwartz BA, Lefebvre A. Contact veille/p.m.o. II. Les P.M.O. morcelles. Rev Electroencephalogr Neurophysiol Clin 1973;3: Hishikawa Y, Sumitsugu N, Matsumoto K, Kaneko Z. H-reflex and EMG of the mental and hyoid muscles during sleep, with special reference to narcolepsy. Electroencephalogr Clin Neurophysiol 1965;18: Hodes R, Dement WC. Depression of electrically induced reflexes ("H-reflexes") in man during low voltage EEG sleep. Electroencephala/?r Clin NeurophysioI1964;17: Pivik R, Metz J. Phasic EMG inhibition and spinal reflex modulation during synchronized sleep in the cat. Exp Neural 1975;48: Pivik R, Metz J. Spinal and lateral geniculate nucleus activity during sleep: quantitative relationships. Exp NeuroI1982;77: Rechtschaffen A, Kales A, eds. A manual of standardized terminology, techniques, and scoring system for sleep stages of human subjects. Los Angeles: University of California at Los Angeles, Brain Information Service/Brain Research Institute, Magladery J, McDougal G. Electrophysiologic studies of nerve and reflex activity in normal man. I. Identification of certain reflexes in the electromyogram and the conduction of peripheral nerve fibers. Bull Johns Hopkins Hosp 1950;86: Magladery J, Teasdale R, Park A. Electrophysiologic studies of nerve and reflex activity in patients with lesions of the nervous system: a comparison of spinal motorneuron excitability following afferent nerve volleys in normal persons and patients with upper motor neuron lesions. Bull Johns Hopkins Hosp 1952;91 :