The Concurrence of Fine Muscle Activity and Rapid Eye Movements During Sleep

Transcription

1 The Concurrence of Fine Muscle Activity and Rapid Eye Movements During Sleep BILL J. BALDRIDGE, B.A., ROY M. WHITMAN, M.D., and MILTON KRAMER, M.D. Body movements were detected by means of highly sensitive semiconductor strain gauges on 10 subjects who slept overnight in a dream laboratory. Continuous measurement of movement from the eye, throat, hand, and foot indicated that activation was an integrated process which appears simultaneously from all locations. Correlations of level of eye movement activity and average activity level from other points measured ranged between.55 and.85 for each of 10 subjects, with the majority exceeding.75. Body movement patterns correctly identified 32 of 41 peats of eye movement activity. A N 1953, Aserinsky and Kleitman 1 reported the occurrence of rapid eye movements during sleep similar to visual scanning movements made when awake. These eye movements, they found, bore a definite relation to time of dreaming, enabling them to identify three to five dream periods per night. Other investigators, including Dement and Kleitman, 7 Dement and Wolpert, 9 and Roffwarg et al., 1 * have substantiated this finding and further have reported that the num- From the Department of Psychiatry, University of Cincinnati College of Medicine and the Veterans Administration Hospital, Cincinnati, Ohio. This study was supported by Research Grant MH from the National Institute of Mental Health, U. S. Public Health Service, and was presented in part at the seventy-first meeting of the American Psychological Association in Philadelphia. Received for publication Apr. 16, ber and direction of eye movements correspond to the movement in the dream. Dement and Kleitman 0 ' 8 made the observation that eye movements occur only during EEG Emergent Stage 1 and suggested the EEG as a more reliable indicator of time of dreaming, noting that dreams may occur in which little or no movement takes place. At the time of discovering that the eye muscles were active during dreaming, Aserinsky and Kleitman also noted the cyclic occurrence of gross body movements. In their original report they stated: "In every case the eye motility periods were associated with peaks of overt body activity... Z' 1 In 1955, however, they reported that eye movements were seen to persist for several minutes in the absence of body movements. 3 In a later paper, Dement and Kleitman 8 commented that the rise of incidence of

2 20 EYE MOVEMENT AND MUSCLE ACTIVITY gross body movements with EEG peaks was somewhat misleading. They found the rapid eye movement period often started after a series of body movements and might terminate with a body movement, but that the sleeping subject seemed relatively quiet during the dream period. Body movements were reported to rise to a peak but drop sharply at the onset of eye movements and to rise again after the eye movements ceased. Dement and Wolpert 9 and Wolpert and Trosman 18 have also reported the occurrence of gross body movements at the termination of a dream period or as interrupting a dream episode in a multiple-scene dream. Dement and Kleitman 8 noted an increase of fine muscle movements during the dream phase which was almost completely absent at other times. These fine movements were detectable by direct observation but frequently failed to be recorded with the method of detection used in their study. Dement and Wolpert, 9 in studying body movement and dreaming, reported it seemed somewhat paradoxical that eye movements followed the course of the dream while body movements did not and suggested that one should expect to observe at least rudimentary movements of the limbs during dreaming. In perhaps what was the first study designed specifically to test for presence of fine muscle movements during dreaming, Wolpert 15 observed a greater incidence of isolated movements (wrist and leg) during the dream period, but found no difference in the incidence of combined movements between the dream and the nondrearn period. He found the occurrence of fine muscle movements corresponded with reported dream activity but also noted several dreams which were unaccompanied by electromyographic activity. Berger 8 has reported a striking decrease in muscle tonus at the onset of each period of light sleep with rapid eye movements and dreaming, while Fischgold and Schwartz 10 have suggested the contrary to be true since snoring, which depends on the relaxing of the oropharyngeal muscles, rarely occurs during dreaming. Sleep talking has been reported to occur at all times of the night and during both rapid eye movement and nonrapid eye movement. 13 Selecting at random one sleep-talking incidence from each of 28 subjects the distribution was 14% from rapid eye movement periods and 84% from EEG Stages 2, 3, and 4. From these studies it may be seen that no clear over-all picture of muscle activity during the night is available. In particular, the extent and pattern of fine movement during the night has not been clearly specified. An examination of the methods of recording and reporting which have been used reveals much of the cause of this deficiency. In the studies by Aserinsky and Kleitman and Dement and Kleitman, activity was scored as the number of 5-min. segments within each successive 30-min. period in which any movement occurred. Thus two 30-min. periods could have been scored 6, indicating maximum movement, even though there was included a period of quiescence of just less than 10 min. In a like manner, two adjacent 30-min. periods could each have received a score of 5 though they included a quiescent period of nearly 20 min. Wolpert 15 stated; "There can be no doubt that appropriate but reduced motor activity' of both extraocular and somatic musculature accompanies dreaming." Yet, when he tested this hypothesis by subject, only 1 of 8 showed a chance probability of occurrence of less than.05. It should also be noted that more than 40% of the dream awakenings were eliminated because of inadequate EMG recording or lack of recall of last dream item. Berger 5 reported a decrease in laryn- PSYCHOSOMATIC MEDICINE

3 BALDRIDGE ET Al. 21 geal-muscle tone during dreaming. In this report he also referred to the occurrence of momentary increases of muscle activity due to swallowing, etc., but did not elaborate on this observation. It is believed the differences of observed movement during sleep and dreaming have resulted from this great variety of conditions, methods, and objectives of the respective studies. Preliminary observations of body movements, using sensitive strain gauges as detectors, led to the prediction that periods of dreaming with eye movements would always be accompanied by widespread and nearly continuous fine-movement activity from the total body musculature. Procedure To test the hypothesis, body movement records were collected from 10 paid volunteer subjects who slept overnight in a dream laboratory. They were told only that the study was concerned with, movements during sleep. The subjects slept in a privatetype hospital room and, after the initial attachment of the instrumentation, were undisturbed throughout the night. While the subjects slept, continuous recordings of movement were made from the eye, throat, wrist, and ankle of each." Movement from each of the four locations was detected by a highly sensitive semiconductor strain gauge described previously in this journal 4 Attachment of the strain gauge to the subject's eyelid and the other locations indicated was made by means of a small piece of adhesive tape. The strain gauge produced only a minimum of interference with the normal opening of the eye and no interference with other movements. Sensitivity of the measurements was such that eye movements of about 2 degrees and other movements which were barely perceptible by direct observation could be distin- * Records collected from several exploratory nights showed other locations such as the upper arm, shoulder, and abdomen to produce results comparable to those from locations \ised in collecting the data reported here. VOL XXVII, NO. I, 1965 guished on the record. The output from each of the strain gauges was recorded on a Grass Model 5 polygraph at a chart speed of.5 mm./sec. A check of the response of each of the strain gauge placements was made at the beginning of each night at a chart speed of 25 mm./sec. to insure their independent operation and to check operating sensitivity. Figure 1 presents a record of one such test in which the subject was instructed to make the smallest possible voluntary movement of his eye, throat, wrist, and ankle. The independence of the strain gauge action may be seen as well as the signal-to-noise ratio. Results Periods of activity and quiescence occurred alternately throughout the night on every record. During the periods of activity movement was always recorded from two or more channels. Isolated movements from a single channel were observed on many occasions but once a sustained activity appeared it was nearly always present in all channels. Differences in frequency of movement from the four channels were produced by a number of factors: (1) only a cursory attempt was made to equate sensitivity among the various placements of the strain gauges; (2) it is probably true that fine body movements are in some way related to activity in the dream as reported by Wolpert, and (3) movement from the various parts of the body are grossly affected by body position of the sleeping subject. Periods of quiescence were observed to last from a few minutes to an hour or more. Numerous records were observed in which as few as isolated movements were recorded from all channels over a period of min. (It should be recalled that the sensitivity of the recording was such that the slightest voluntary movements were recorded.) During one long quiescent period, no indication of movement was recorded from the

4 11 EYE MOVEMENT AND MUSCLE ACTIVITY four channels for more than 50 min. At other times gross movements interrupted the periods of quiet at intervals ranging from a few seconds to several minutes. These were almost always seen as a large amplitude excursion occurring in all channels simultaneously. Their duration varied but usually continued for only a few seconds without interruption. Artifacts of pulse and breathing occurred from time to time in all channels but were distinguished from movements by their periodic nature and frequency. An example of an activity cycle consisting of a 90-min. period from the record of one subject is shown in Fig. 2. The sequence begins during a period of quiescence, shown in the first row, with only an isolated indication of movement from the throat and ankle. Near the end of the first row, what appears to be a gross body movement occurs preceding the period of rapid eye movement. The second row shows a high level of activity from all four channels throughout this 30-min. period. The activity period is followed by a return to quiescence in the third row. The all-night records of each of the 10 subjects were divided into 10-min. segments for analysis. Each 10-min. segment was further subdivided into 1-min. intervals and examined for movement activity. The number of 1-min. intervals showing any activity during each 10-min. segment was designated the activity density for that period. The activity density, which could range from 0 to 10, was determined for each of the four channels. A plot of the activity density measured from the eye and the average of the activity from the throat, wrist, and ankle of one subject over an entire night are shown in Fig. 3. Eye. Throat Wrist Ankle FIG. 1. Polygraph record showing sensitivity and independence of operation of strain gauge placements. PSYCHOSOMATIC MEDICINE

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6 24 EYE MOVEMENT AND MUSCLE ACTIVITY Minute Periods FIG. 3. Activity density plot for eye movement and average density of movement from throat, wrist, and ankle. Density is plotted as number of 1-min. periods showing activity in each 10-min. interval. When the records had been transposed into sets of activity density, those from the throat, wrist, and ankle were summed for each 10-min. segment. The resulting sums were correlated, by means of a Pearson product-moment correlation, with the activity density of the eye movement The correlations for each of the 10 subjects, shown in Table 1, ranged from.55 to.85, with the majority being above.75. These correlations were all 3-5 times the standard error for an assumed zero correlate. A second form of analysis was also performed to determine the accuracy with which eye movement periods could be detected by body movements. The data for each subject were plotted as in Fig. 3, except that eye movement density and body movement density were TABLE 1. CORRELATION BY SUBJECTS BETWEEN EYE MOVEMENT AND BODY ACTIVITY WITH STANDABD ERBOB FOB AN ASSUMED CORRELATION OF ZERO & RR DS MA DC JuC SL PS BS JH JC r GO JV or plotted on separate graphs. Eliminating the first 100 min. of each subject night as a period for going to sleep, there were judged to be 41 peaks of eye movement activity among the 10 subject nights. Peaks of body movement activity were found to identify 32 of these periods when activity level was determined from body movement alone. Two activity periods were indicated by body movements which were not indicated by eye movements. Discussion Two striking features were observed in the sleeping records of the 10 experimental subjects. The first was the degree to which fine body movements occurred concomitantly with eye movements throughout the eye movement period; the second was the almost complete absence of all activity during the periods of quiescence. The periodic variations of motility have been referred to a number of times, yet no adequate description has been presented. Aserinsky and Kleitman 1 " 3 reported on cyclic activity primarily in relation to the cycle length and the relation of eye motility with peaks of body movement. 1 ' s - fl These authors generally were referring to gross body movement; however, little information was presented on the sensitivity of the measurements made. Dement and Kleitman 3 presented motility data which consisted PSYCHOSOMATIC MEDICINE

7 BALDRIDGE ET Al. 25 of the average motility for a number of subject nights; thus, individual periods of activity and quiescence were obscured. In addition, they noted that all observable movements were not being recorded. Dement and Wolpert 9 made reference to body movement in relation to the beginning and end of a dream or to its interruption but referred specifically to gross body movements. Wolpert, 10 in his study of movement during dreams, made no direct reference to a cyclic active and inactive pattern. The marked contrast between the active and quiescence phase observed in the present study strongly supports the possibility of two distinct mechanisms or types of sleep in human subjects as described by Jouvet in the cat. 11 Since subjects were not awakened during eye movement periods for positive verification of dreaming, the concurrence of dreaming with the movements recorded may only be inferred. The likelihood that dreaming was occurring, however, is quite high. Several early studies making use of rapid eye movements only, produced positive dream reports from about 80% of the awakenings from eye movement periods. 1 - :i - 8 ~ s Dement and Kleitman, s while suggesting that Emergent Stage 1 EEG should be a more positive indicator of dreaming, specified that the occurrence of rapid eye movements was used as the objective indicator of dreaming. These authors reported the sensitivity of their eye movement recording to be about 100 mv for an eye movement of 20 degrees. Detection of eye movement by a strain gauge has been shown to be many times more sensitive than that recorded by means of the corneoretinal potential. 4 In addition, several hundred nights of dreaming with awakenings have been monitored using a single strain gauge, and have resulted in a number of dreams per night and a percentage of positive dream reports comparable to those obtained by the EEG-eye movement method. VOL. XXVII, NO. I, 1965 The mechanism responsible for the cyclic occurrence of fine body movements is not known. Kleitman 12 has presented evidence for a basic activation cycle which extends throughout both sleep and wakefulness. The concurrence of fine body movements with dreaming would suggest three interesting possibilities: (1) movement during the dream is an attempt on the part of the dreamer to carry out the action of the dream as it unfolds; (2) movements occur spontaneously, providing an increased proprioceptive input to the cortex which is then interpreted as a dream; or (3) both the dream and the muscle activity occur simultaneously as a result of separate activating mechanisms, perhaps in the reticular formation. Department of Psychiatry Cincinnati General Hospital Cincinnati, Ohio References 1. ASEBINSKY, E., and KLEITMAN, N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118:273, ASEBINSKY, E., and KLETTMAN, N. A motility cycle in sleeping infants as manifested by ocular and gross bodily activity. ]. Appl. Physiol. 8:11, ASEBINSKY, E., and KLEITMAN, N. TWO types of ocular motility occurring in sleep. /. Appl. Physiol. 8:1, BALDBIDGE, B. J., WHITMAN, R. M., and Kramer, M. A simplified method for detecting eye movements during dreaming. Psychosom. Mecl. 25:78, BERGER, R. Tonus of extrinsic laryngeal muscles during sleep and dreaming. Science 134:840, DEMENT, W., and KLEITMAN, N. Incidence of eye motility during sleep in relation to varying EEG patterns. Fed. Proc. 14:216, DEMENT, W., and KLEITMAN, N. The relation of eye movements during sleep to dream activity: an objective method

8 26 for the study of dreaming. /. Exper. Psychol. 53:339, DEMENT, W., and KLEITMAN T, N. Cyclic variations in EEG during sleep and their relation to eye movements, body motility and dreaming. Electroencephalog. ir Clin. Neurophysiol. 9:673, DEMENT, W., and WOLPERT, E. The relation of eye movements, body motility, and external stimuli to dream content. /. Exper. Psychol. 55:543, FISCHCOLD, H., and SCHWAUTZ, B. "Sleep in the Human Adult." In G.E.W. Wolstenholme and M. O'Conner (Eds.), The Nature of Sleep. Little, Boston, ] 1. JOUVET, M. "Telecephalic and Rhombencephalic Sleep in the Cat." In EYE MOVEMENT AND MUSCLE ACTIVITY G.E.W. Wolstenholme and M. O'Conner (Ed.), The Nature of Sleep. Little, Boston, KLEITMAN, N. Sleep and Wakefulness. Univ. Chicago Press, Chicago, RECHTSCHAFFEN, A., GOOUENOUCH, D., and SHAPIRO, A. Patterns of sleep talking. Arch. Gen. Psychiat. 7:418, ROFFWABG, H., DEMENT, W., MUZIO, J., and FISHER, C. Dream imagery: relationship to rapid eye movements of sleep. Arch. Gen. Psychiat. 7:235, WOLPERT, E. Studies in psychophysiology of dreams II. Arch. Gen. Psychiat. 2:231, WOLPEHT, E., and TKOSMAN, H. Studies in psychophysiology of dreams. Arch. Neurol. Psychiat. 79:603, PSYCHOSOMATIC MEDICINE