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Relationship of intrauterine fetal activity to maternal sleep stage
98
STERMAN BILATERAL
INTERTHALAMIC
COHERENCE AWAKE
1.0 ,
OF DORSAL
MEDIAL
NUCLEI
IN MAN:
AND ASLEEP
.:I ,,,,,,,,,,,,, 4
6
6
0
12
FREOUEMCY
I4
16
Y CYCLES
1 I6
20
22
24
26
26
30
PER SECOND
FIG. 40. Chart of coherences found, at all frequencies of the spectrum, between the dorsal medial nuclei of the thalamus in the two hemispheres in a nonepileptic patient. Coherences above 0.26 are statistically significant.
The EEG’s from which these computer analyses were made were mostly from all-night recordings, and the sampling from time to time for calculations showedconsiderable fluctuation in the coherencevalues. Whether these related in any way to the presenceor absenceof dreaming is not known to us for the patients were not awakened and interrogated. Since the goal of the workshop is an exploration of possible physiological correlates of dreaming, the present report is offered as an approach to the examination of brain mechanismsthat may underlie one of the reasonsfor failure to report a dream.
Relationship
of Intrauterine Maternal Sleep
Fetal Stage
Activity
to
M. B. STERMAN Los
Angeles,
California
It has long been theorized that some substance accumulating within the blood precipitates the phenomenon of sleep, and recent developments in the field of sleep research have led to renewed pursuit of the elusive “hypnotoxin.” In addition to advances in neurophysiological concepts of sleep, there
CORRELATES
OF
DREAMING
99
has been the recognition of two distinct physiological sleep patterns, one of which, besides being associated with the psychic phenomenon of dreaming in man, is characterized by the occurrence of rapid eye movements and a variety of physiological irregularities. The characteristics of the so-called slow wave (SW) and rapid eye movement (REM) stages of sleep are well known today, but it is appropriate in the present context to reiterate the fact that REM sleep is associated with a variety of tonic and phasic peripheral manifestations indicative of a widespread expression of some fundamental change within the organism. The diffuse onset and termination of these phenomena would not be inconsistent with a systemic rather than neural mediation. The hemo-chorial placenta of man and other primates provides an intimate contact between the maternal and fetal circulations. Except for the housing of the fetus within the maternal uterus, this is the exclusive route of communication between these two physiological systems. This fact was exploited in the present study in an effort to assess the possible contribution of systemically transported substances to the mediation of REM sleep in man. Attempting to compare the sleep stages of a mother and her fetus presented difficult technical problems. While it is a simple matter to register the sleep stage of the mother through the use of well-established electrophysiological recording techniques, the inaccessibility of the fetus makes a similar approach impossible for this member of the unit. However, studies of the sleep of newborn infants provided a solution to this problem. A consistent feature of REM sleep in the newborn is the occurrence of an almost continuous sequence of muscle contractions, including twitches of the face and extremities interspersed with gross changes in the position of the limbs and trunk ( 160, 183). This is in marked contrast to the quiescent nature of SW sleep, which is almost entirely devoid of muscular activity. If we assume that these two sleep states are distinguished by a similar dichotomy in somatic activity during advanced fetal life, it is possible to approximate fetal sleep directly by recording unprovoked fetal activity during maternal sleep. A preliminary description of the relationship between maternal sleep and fetal activity has been presented elsewhere (204), and a more complete analysis than can be presented here will be forthcoming. Methods. Multiple recording sessions were carried out on five women, ranging in age from 22 to 28 years, during the last four calendar months of pregnancy. Each subject was exposed to laboratory sleeping conditions prior to the first of at least three experimental recording nights. They reported to the laboratory at their normal retiring hour, were prepared for physiological monitoring, and allowed to sleep until 8 A.M. the following morning. Continuous EEG, EMG, and eye movement recordings were obtained from the mother through use of the techniques described by Jacob-
100
STERMAN
son et al. ( 115). Fetal activity was monitored by the application of pressuresensitive devices to the abdominal surface. The position of the fetus was first estimated by Leopold maneuvers and by the mother’s localization of fetal kicking. Three 24 inch speakers, fitted with flexible plastic diaphragms over the open end of the acoustic cone, were taped to the abdomen over the fetal head, limbs, and buttock, respectively (Fig. 4 1) . An additional speaker
FIG. 41. Illustration of electrode placement for recording of fetal activity. electrode was placed on the dorsal surface of the thigh in order to differentiate activity.
Control maternal
was applied to the dorsal surface of the thigh. Leads from these devices were connected to four Grass DC amplifiers. Pressure changes produced by fetal movements were displayed together with maternal EEG, EMG, and eye movement records on a lo-channel Grass polygraph (Fig. 42). Body movements on the part of the mother were detected in recordings obtained from the thigh electrode and from EEG and submental muscle leads on the head. Respiration was occasionally monitored by attaching a pneumatic strain gauge, through a transducer, to a DC recording channel. At the beginning of each experimental night the subject was asked to perform certain body movements and to report fetal activity in order to provide additional experimental information. Recording gains were adjusted to register a low and consistent level of background physiological activity.
CORRELATES
OF
101
DREAMING
Maternal sleep was classified according to the criteria of Dement and Kleitman (54). Since desynchronization of the EEG, loss of submental muscle tone, and onset of REM’s rarely occurred or terminated simultaneously, there was seldom a discrete demarcation of REM sleep. A conservative definition was established that required the simultaneous presence of these epiphenomenafor the classification of REM sleep. Thus, the period defined ,.I
.,I
VERTEX-LFT. TRANS. FR. VERTEX-RT TRANS.
FRP
)*
,...I,,. OCC."
OCC.
p
EYES SUBMENTAL FUAL : HEAD
lu ----&-
BUTTOCK LEGS CONTROL(THIGH)
---4---v.. i'n,
,i
FIG. 42. Polygraphic display of electrophysiological recordings from mother and fetus. The two upper sets of tracings show differentiation of fetal movements from artifacts induced by maternal activity during REM sleep. Lower set of tracings show an example of the record obtained during fetal hiccup. The latter was never seen during Stages 3 and 4 or ascending Stage 1 of sleep.
as REM sleep here does not consider those adjacent segments of record which often show several of its characteristics. The electrical recordings of fetal activity indicated several different types of movement, including kicks, squirming, general agitation, and fetal hiccup. The latter consists of a prolonged period of rhythmic jerks (see Fig. 42) associatedwith hiccup by previous investigators (219). Since these periods of activity may be related to influences outside the realm of interest in the present study, they were excluded from the analysis performed here. In this analysis, each distinct episode of movement, regardless of its nature, was
102
STERMAN
classified as one movement. These were then quantified and expressed as either the total number of movements during a unit of time, or the mean number of movements per 20-min interval. Test observations of the mother at the beginning of each recording session indicated that neither previous activity nor a variety of body movements influenced the fetal activity recorded from a ye&zing mother. This is in agreement with similar observations reported by a number of other investigators (96, 178, 185). Sub., S.P. 7mo. REM
40 2 i:
F
35
0
SLEEP ONSET
TIME
IN HOURS
FIG. 43. Distribution of fetal movements during a night of maternal sleep. Mother’s REM sleep episodes are labeled at the top. Brief awakenings during the night have no systematic effect upon fetal activity, but marked increases are seen in relation to two of the four episodes of REM sleep recorded in a .5-hour sleep observation.
Results. The fetal activity recorded from a given subject over three or four experimental sessions showed a more or less progressive change toward regularity. Whereas, in midpregnancy, the pattern of fetal activity was diffuse and either spread out rather uniformly throughout the night, or concentrated within certain inconsistent segments of the night, in the last trimester of pregnancy there emerged a rhythmic rest-activity cycle throughout the night. The fetal activity cycle was clearly evident in some subjects and less so for others, the variability probably resulting from differences in fetal position within the uterus leading to differences in the adequacy of recording. Cycle time ranged from 40 min when discernable at 5-6 months gestation age to
CORRELATES
OF
103
DREAMING
60 min near term. This trend was consistent, in spite of the variability observed. In every subject studied there were numerous episodes of REM sleep accompanied by very specific increases in fetal motility. Typically, these increases preceded the appearance of REM sleep in the mother, sometimes by as much as 10 min (Fig. 43). Motility was observed to be quite variable throughout the defined period of REM sleep, often showing marked increases
end sleep
0
I hr
I 2hr MATERNAL
A 3hr 4hr SLEEP TIME
5hr
FIG. 44. The distribution of fetal activity, plotted per 200 set, is shown during two nights of maternal sleep in this figure. Note the more cyclic nature of baseline fetal activity in the recording obtained at 8 months of pregnancy. In the recording obtained at 7 months, three of the four REM sleep episodes are associated with increased fetal motility. No special increases were observed in the S-month recording. However, two of the episodes are concurrent with the onset of activity preceded by periods of relative quiescence.
in relation to a burst of brisk eye movements and equally marked decreases during prolonged periods of ocular quiescence. In some instances, maximal increases in fetal motility were observed to occur after the termination of REM sleep (Figs. 44 and 45). Specific changes were least often seen during the first sleep cycle of the night. In this regard it is interesting to recall that the first REM sleep episode of the night in man is characteristically diffuse and often lacks several of the basic epiphenomena of this sleep pattern (136). Episodes of REM sleep at the end of the night were less likely, also, to be associated with substantial increases in fetal activity.
104
STERMAN
A determination of the exact relationship between maternal REM sleep and fetal motility requires a quantitative evaluation of the interaction between endogenous fetal activity and the influences of maternal sleep. Such an evaluation is not available at the present time. From a general analysis Sub. A.M.,7ma 4.0-
R.S.
U.S.
3.0 -
2.0l.O0 6”.
I 60
30 YIN fE?IlL HICCUP 1 B-m I 120
“%? NlCCUf 1 / /v 180
/I I 300
240
I 360
Sub. A.M.,Sma R.S.
4.0 -
R.S.
3.0 -
2.0-
“F;E HICCUP
/VI 0
60I
v I 120
I80I
% I 240
Ai I 300
I 360
300
360
Sub. A.M., 8.5 ma 4.0
3.0
2.0
I .o
0
60
120
I80
TIME
240
IN MINUTES
FIG. 45. Comparison of mean fetal activity, during three nights of maternal sleep in same subject. Recordings obtained during the seventh month of pregnancy and at the beginning of the eighth month show a disturbance of sleep reflected by decreased REM sleep and prolonged sleep cycle time. By 8.5 months of pregnancy the sleep pattern appeared to be more normal. Note the corresponding absence of peaks in fetal activity during the earlier recordings. the
of the data one must conclude that there is no definite evidence for a direct relationship. It is possible to state, however, that in 61% of the REM sleep episodes recorded, a progressive or specific increase in fetal motility was observed. A clarification of this relationship awaits further data. An examination of sequential observations from the same subject dis-
CORRELATES
OF
DREAMING
105
closed moderate changes in the sleep cycle during the course of pregnancy. In the last trimester there is increasing discomfort for the mother, which is reflected in her sleep by an extension of sleep cycle time related to a decrease in REM sleep time. Sleep patterns often returned to normal during the last month of pregnancy (Fig. 44). Discussion. The development of a rhythmic rest-activity cycle in the fetus of a sleeping mother suggests that intrauterine life under such conditions can consist primarily of recurrent periods of quiet and active sleep. The cycle values obtained agree with extrapolated predictions based upon the observed active and quiet sleep cycle of premature and fullterm infants (183). The occurrence of REM sleep in the mother may interrupt this baseline activity and impose upon it significant increases in fetal motility. These increases, when they occur, are often manifest some time in advance of the onset of maternal REM’s. Such a pattern resembles active sleep as described in neonates by Roffwarg et al. (179). As quiet sleep yielded to active sleep in these infants, continuous twitches, grimaces, tremors, and athetoid movements of the limbs appeared up to 10 min before the onset of REM?. Movements dropped off gradually at the end of such a period. Since a potential maternal influence is not a function of maternal motility, it must reflect some changed aspect of the two intimately associated circulations. We could speculate that a substance constituting the biochemical basis of REM sleep is released into the circulation, and, depending upon the intensity of the episode, can reach high enough levels to impose upon the independent sleep cycle of the fetus. On the other hand, the physiological activation characteristic of the mother’s REM sleep episode may lead to endocrine changes which succeed in merely awakening a sleeping fetus. In either case, it is apparent that the humoral influence, regardless of its functional nature, can be expressed substantially in advance of and following the more overt characteristics of this sleep phase in the mother. Fetal activity has been experimentally increased by interruptions of the placental circulation leading to asphyxia, and by any transection of the neuraxis between the diencephalon and upper cervical cord (13). Sontage (202) stated that marked fear or conditions of prolonged maternal emotionality also increase fetal activity in humans. He points out, further, that changes in maternal endocrine output can alter the state of the fetus by virtue of the so-called “endocrine pool” existing between the mother and her fetus. Therefore, it is possible that the dynamics observed here are mediated by changes in blood gas levels or by compensatory endocrine responses in the fetus. The interaction between maternal and fetal physiology may account for the variations observed. On another level, it is possible that physiological changes initiated by hallucinated emotions during dreaming can sometimes cause an indirect excitation of the fetus. A basic problem with this interpretation touches
106
HERNANDEZ-PE6N
upon one of the fundamental discrepancies in the entire “dream sleep” story. This is the well-demonstrated fact that all of the peripheral manifestations of REM sleep demonstrate a frequent independence from the basic EEG desynchronization so important to the concept of dreaming. In the case of induced fetal activity, we again see a discrepancy in this regard. One could say, with equal validity, that fetal activity or decreased muscle tone or rapid eye movements induce dreaming. The results of this investigation suggest that we have yet another fertile field for investigation regarding the mechanism, function, and significance of REM sleep. Summary. An attempt was made to evaluate the possibility of a humoral, rather than neural, mediation of the epiphenomena of REM sleep. The exclusively systemic communication between a mother and her fetus provided a readily available preparation for an initial approach to this problem. With reference to the sleep of newborn infants, it was assumed that periods of active motility in the fetus of a sleeping mother reflected the occurrence of REM sleep in this organism. Maternal sleep was monitored by standard recording procedures, and fetal sleep was inferred from recordings of intrauterine activity. The following results were obtained from comparisons of all-night sleep records of the mother-fetus unit: (a) The fetus tends to develop a recurrent quiet-active cycle in the course of gestation. (b) Specific instances of high fetal activity frequently occur together with or in close proximity to the recurrent episodes of REM sleep in the mother. Such increases, when they occur, appear to be related to the appearance of maternal REM sleep; however, they are not a systematic feature of this sleep phase. (c) A number of potential mechanisms for a dynamic humoral communication between the two physiological units during REM sleep are discussed.
Neurophysiology, Phylogeny, and Significance of Dreaming RAUL Mexico
Functional
HERNANDEZ-F'E~N~ City,
Mexico,
D.F.
Although the origin and significance of dreams have attracted human curiosity since ancient times, it has been only in the last few years that an experimental approach to this problem with neurophysiological methodology promises a scientific understanding of the pervasive oneiric experiences. 1 The investigation reported in this paper was supported by the National Mental Health, U.S. Public Health Service, under Grant MH 10003-03, Foundation’s Fund for Research in Psychiatry under Grant 66-340.
Institute and by
of the
STERMAN BILATERAL
INTERTHALAMIC
COHERENCE AWAKE
1.0 ,
OF DORSAL
MEDIAL
NUCLEI
IN MAN:
AND ASLEEP
.:I ,,,,,,,,,,,,, 4
6
6
0
12
FREOUEMCY
I4
16
Y CYCLES
1 I6
20
22
24
26
26
30
PER SECOND
FIG. 40. Chart of coherences found, at all frequencies of the spectrum, between the dorsal medial nuclei of the thalamus in the two hemispheres in a nonepileptic patient. Coherences above 0.26 are statistically significant.
The EEG’s from which these computer analyses were made were mostly from all-night recordings, and the sampling from time to time for calculations showedconsiderable fluctuation in the coherencevalues. Whether these related in any way to the presenceor absenceof dreaming is not known to us for the patients were not awakened and interrogated. Since the goal of the workshop is an exploration of possible physiological correlates of dreaming, the present report is offered as an approach to the examination of brain mechanismsthat may underlie one of the reasonsfor failure to report a dream.
Relationship
of Intrauterine Maternal Sleep
Fetal Stage
Activity
to
M. B. STERMAN Los
Angeles,
California
It has long been theorized that some substance accumulating within the blood precipitates the phenomenon of sleep, and recent developments in the field of sleep research have led to renewed pursuit of the elusive “hypnotoxin.” In addition to advances in neurophysiological concepts of sleep, there
CORRELATES
OF
DREAMING
99
has been the recognition of two distinct physiological sleep patterns, one of which, besides being associated with the psychic phenomenon of dreaming in man, is characterized by the occurrence of rapid eye movements and a variety of physiological irregularities. The characteristics of the so-called slow wave (SW) and rapid eye movement (REM) stages of sleep are well known today, but it is appropriate in the present context to reiterate the fact that REM sleep is associated with a variety of tonic and phasic peripheral manifestations indicative of a widespread expression of some fundamental change within the organism. The diffuse onset and termination of these phenomena would not be inconsistent with a systemic rather than neural mediation. The hemo-chorial placenta of man and other primates provides an intimate contact between the maternal and fetal circulations. Except for the housing of the fetus within the maternal uterus, this is the exclusive route of communication between these two physiological systems. This fact was exploited in the present study in an effort to assess the possible contribution of systemically transported substances to the mediation of REM sleep in man. Attempting to compare the sleep stages of a mother and her fetus presented difficult technical problems. While it is a simple matter to register the sleep stage of the mother through the use of well-established electrophysiological recording techniques, the inaccessibility of the fetus makes a similar approach impossible for this member of the unit. However, studies of the sleep of newborn infants provided a solution to this problem. A consistent feature of REM sleep in the newborn is the occurrence of an almost continuous sequence of muscle contractions, including twitches of the face and extremities interspersed with gross changes in the position of the limbs and trunk ( 160, 183). This is in marked contrast to the quiescent nature of SW sleep, which is almost entirely devoid of muscular activity. If we assume that these two sleep states are distinguished by a similar dichotomy in somatic activity during advanced fetal life, it is possible to approximate fetal sleep directly by recording unprovoked fetal activity during maternal sleep. A preliminary description of the relationship between maternal sleep and fetal activity has been presented elsewhere (204), and a more complete analysis than can be presented here will be forthcoming. Methods. Multiple recording sessions were carried out on five women, ranging in age from 22 to 28 years, during the last four calendar months of pregnancy. Each subject was exposed to laboratory sleeping conditions prior to the first of at least three experimental recording nights. They reported to the laboratory at their normal retiring hour, were prepared for physiological monitoring, and allowed to sleep until 8 A.M. the following morning. Continuous EEG, EMG, and eye movement recordings were obtained from the mother through use of the techniques described by Jacob-
100
STERMAN
son et al. ( 115). Fetal activity was monitored by the application of pressuresensitive devices to the abdominal surface. The position of the fetus was first estimated by Leopold maneuvers and by the mother’s localization of fetal kicking. Three 24 inch speakers, fitted with flexible plastic diaphragms over the open end of the acoustic cone, were taped to the abdomen over the fetal head, limbs, and buttock, respectively (Fig. 4 1) . An additional speaker
FIG. 41. Illustration of electrode placement for recording of fetal activity. electrode was placed on the dorsal surface of the thigh in order to differentiate activity.
Control maternal
was applied to the dorsal surface of the thigh. Leads from these devices were connected to four Grass DC amplifiers. Pressure changes produced by fetal movements were displayed together with maternal EEG, EMG, and eye movement records on a lo-channel Grass polygraph (Fig. 42). Body movements on the part of the mother were detected in recordings obtained from the thigh electrode and from EEG and submental muscle leads on the head. Respiration was occasionally monitored by attaching a pneumatic strain gauge, through a transducer, to a DC recording channel. At the beginning of each experimental night the subject was asked to perform certain body movements and to report fetal activity in order to provide additional experimental information. Recording gains were adjusted to register a low and consistent level of background physiological activity.
CORRELATES
OF
101
DREAMING
Maternal sleep was classified according to the criteria of Dement and Kleitman (54). Since desynchronization of the EEG, loss of submental muscle tone, and onset of REM’s rarely occurred or terminated simultaneously, there was seldom a discrete demarcation of REM sleep. A conservative definition was established that required the simultaneous presence of these epiphenomenafor the classification of REM sleep. Thus, the period defined ,.I
.,I
VERTEX-LFT. TRANS. FR. VERTEX-RT TRANS.
FRP
)*
,...I,,. OCC."
OCC.
p
EYES SUBMENTAL FUAL : HEAD
lu ----&-
BUTTOCK LEGS CONTROL(THIGH)
---4---v.. i'n,
,i
FIG. 42. Polygraphic display of electrophysiological recordings from mother and fetus. The two upper sets of tracings show differentiation of fetal movements from artifacts induced by maternal activity during REM sleep. Lower set of tracings show an example of the record obtained during fetal hiccup. The latter was never seen during Stages 3 and 4 or ascending Stage 1 of sleep.
as REM sleep here does not consider those adjacent segments of record which often show several of its characteristics. The electrical recordings of fetal activity indicated several different types of movement, including kicks, squirming, general agitation, and fetal hiccup. The latter consists of a prolonged period of rhythmic jerks (see Fig. 42) associatedwith hiccup by previous investigators (219). Since these periods of activity may be related to influences outside the realm of interest in the present study, they were excluded from the analysis performed here. In this analysis, each distinct episode of movement, regardless of its nature, was
102
STERMAN
classified as one movement. These were then quantified and expressed as either the total number of movements during a unit of time, or the mean number of movements per 20-min interval. Test observations of the mother at the beginning of each recording session indicated that neither previous activity nor a variety of body movements influenced the fetal activity recorded from a ye&zing mother. This is in agreement with similar observations reported by a number of other investigators (96, 178, 185). Sub., S.P. 7mo. REM
40 2 i:
F
35
0
SLEEP ONSET
TIME
IN HOURS
FIG. 43. Distribution of fetal movements during a night of maternal sleep. Mother’s REM sleep episodes are labeled at the top. Brief awakenings during the night have no systematic effect upon fetal activity, but marked increases are seen in relation to two of the four episodes of REM sleep recorded in a .5-hour sleep observation.
Results. The fetal activity recorded from a given subject over three or four experimental sessions showed a more or less progressive change toward regularity. Whereas, in midpregnancy, the pattern of fetal activity was diffuse and either spread out rather uniformly throughout the night, or concentrated within certain inconsistent segments of the night, in the last trimester of pregnancy there emerged a rhythmic rest-activity cycle throughout the night. The fetal activity cycle was clearly evident in some subjects and less so for others, the variability probably resulting from differences in fetal position within the uterus leading to differences in the adequacy of recording. Cycle time ranged from 40 min when discernable at 5-6 months gestation age to
CORRELATES
OF
103
DREAMING
60 min near term. This trend was consistent, in spite of the variability observed. In every subject studied there were numerous episodes of REM sleep accompanied by very specific increases in fetal motility. Typically, these increases preceded the appearance of REM sleep in the mother, sometimes by as much as 10 min (Fig. 43). Motility was observed to be quite variable throughout the defined period of REM sleep, often showing marked increases
end sleep
0
I hr
I 2hr MATERNAL
A 3hr 4hr SLEEP TIME
5hr
FIG. 44. The distribution of fetal activity, plotted per 200 set, is shown during two nights of maternal sleep in this figure. Note the more cyclic nature of baseline fetal activity in the recording obtained at 8 months of pregnancy. In the recording obtained at 7 months, three of the four REM sleep episodes are associated with increased fetal motility. No special increases were observed in the S-month recording. However, two of the episodes are concurrent with the onset of activity preceded by periods of relative quiescence.
in relation to a burst of brisk eye movements and equally marked decreases during prolonged periods of ocular quiescence. In some instances, maximal increases in fetal motility were observed to occur after the termination of REM sleep (Figs. 44 and 45). Specific changes were least often seen during the first sleep cycle of the night. In this regard it is interesting to recall that the first REM sleep episode of the night in man is characteristically diffuse and often lacks several of the basic epiphenomena of this sleep pattern (136). Episodes of REM sleep at the end of the night were less likely, also, to be associated with substantial increases in fetal activity.
104
STERMAN
A determination of the exact relationship between maternal REM sleep and fetal motility requires a quantitative evaluation of the interaction between endogenous fetal activity and the influences of maternal sleep. Such an evaluation is not available at the present time. From a general analysis Sub. A.M.,7ma 4.0-
R.S.
U.S.
3.0 -
2.0l.O0 6”.
I 60
30 YIN fE?IlL HICCUP 1 B-m I 120
“%? NlCCUf 1 / /v 180
/I I 300
240
I 360
Sub. A.M.,Sma R.S.
4.0 -
R.S.
3.0 -
2.0-
“F;E HICCUP
/VI 0
60I
v I 120
I80I
% I 240
Ai I 300
I 360
300
360
Sub. A.M., 8.5 ma 4.0
3.0
2.0
I .o
0
60
120
I80
TIME
240
IN MINUTES
FIG. 45. Comparison of mean fetal activity, during three nights of maternal sleep in same subject. Recordings obtained during the seventh month of pregnancy and at the beginning of the eighth month show a disturbance of sleep reflected by decreased REM sleep and prolonged sleep cycle time. By 8.5 months of pregnancy the sleep pattern appeared to be more normal. Note the corresponding absence of peaks in fetal activity during the earlier recordings. the
of the data one must conclude that there is no definite evidence for a direct relationship. It is possible to state, however, that in 61% of the REM sleep episodes recorded, a progressive or specific increase in fetal motility was observed. A clarification of this relationship awaits further data. An examination of sequential observations from the same subject dis-
CORRELATES
OF
DREAMING
105
closed moderate changes in the sleep cycle during the course of pregnancy. In the last trimester there is increasing discomfort for the mother, which is reflected in her sleep by an extension of sleep cycle time related to a decrease in REM sleep time. Sleep patterns often returned to normal during the last month of pregnancy (Fig. 44). Discussion. The development of a rhythmic rest-activity cycle in the fetus of a sleeping mother suggests that intrauterine life under such conditions can consist primarily of recurrent periods of quiet and active sleep. The cycle values obtained agree with extrapolated predictions based upon the observed active and quiet sleep cycle of premature and fullterm infants (183). The occurrence of REM sleep in the mother may interrupt this baseline activity and impose upon it significant increases in fetal motility. These increases, when they occur, are often manifest some time in advance of the onset of maternal REM’s. Such a pattern resembles active sleep as described in neonates by Roffwarg et al. (179). As quiet sleep yielded to active sleep in these infants, continuous twitches, grimaces, tremors, and athetoid movements of the limbs appeared up to 10 min before the onset of REM?. Movements dropped off gradually at the end of such a period. Since a potential maternal influence is not a function of maternal motility, it must reflect some changed aspect of the two intimately associated circulations. We could speculate that a substance constituting the biochemical basis of REM sleep is released into the circulation, and, depending upon the intensity of the episode, can reach high enough levels to impose upon the independent sleep cycle of the fetus. On the other hand, the physiological activation characteristic of the mother’s REM sleep episode may lead to endocrine changes which succeed in merely awakening a sleeping fetus. In either case, it is apparent that the humoral influence, regardless of its functional nature, can be expressed substantially in advance of and following the more overt characteristics of this sleep phase in the mother. Fetal activity has been experimentally increased by interruptions of the placental circulation leading to asphyxia, and by any transection of the neuraxis between the diencephalon and upper cervical cord (13). Sontage (202) stated that marked fear or conditions of prolonged maternal emotionality also increase fetal activity in humans. He points out, further, that changes in maternal endocrine output can alter the state of the fetus by virtue of the so-called “endocrine pool” existing between the mother and her fetus. Therefore, it is possible that the dynamics observed here are mediated by changes in blood gas levels or by compensatory endocrine responses in the fetus. The interaction between maternal and fetal physiology may account for the variations observed. On another level, it is possible that physiological changes initiated by hallucinated emotions during dreaming can sometimes cause an indirect excitation of the fetus. A basic problem with this interpretation touches
106
HERNANDEZ-PE6N
upon one of the fundamental discrepancies in the entire “dream sleep” story. This is the well-demonstrated fact that all of the peripheral manifestations of REM sleep demonstrate a frequent independence from the basic EEG desynchronization so important to the concept of dreaming. In the case of induced fetal activity, we again see a discrepancy in this regard. One could say, with equal validity, that fetal activity or decreased muscle tone or rapid eye movements induce dreaming. The results of this investigation suggest that we have yet another fertile field for investigation regarding the mechanism, function, and significance of REM sleep. Summary. An attempt was made to evaluate the possibility of a humoral, rather than neural, mediation of the epiphenomena of REM sleep. The exclusively systemic communication between a mother and her fetus provided a readily available preparation for an initial approach to this problem. With reference to the sleep of newborn infants, it was assumed that periods of active motility in the fetus of a sleeping mother reflected the occurrence of REM sleep in this organism. Maternal sleep was monitored by standard recording procedures, and fetal sleep was inferred from recordings of intrauterine activity. The following results were obtained from comparisons of all-night sleep records of the mother-fetus unit: (a) The fetus tends to develop a recurrent quiet-active cycle in the course of gestation. (b) Specific instances of high fetal activity frequently occur together with or in close proximity to the recurrent episodes of REM sleep in the mother. Such increases, when they occur, appear to be related to the appearance of maternal REM sleep; however, they are not a systematic feature of this sleep phase. (c) A number of potential mechanisms for a dynamic humoral communication between the two physiological units during REM sleep are discussed.
Neurophysiology, Phylogeny, and Significance of Dreaming RAUL Mexico
Functional
HERNANDEZ-F'E~N~ City,
Mexico,
D.F.
Although the origin and significance of dreams have attracted human curiosity since ancient times, it has been only in the last few years that an experimental approach to this problem with neurophysiological methodology promises a scientific understanding of the pervasive oneiric experiences. 1 The investigation reported in this paper was supported by the National Mental Health, U.S. Public Health Service, under Grant MH 10003-03, Foundation’s Fund for Research in Psychiatry under Grant 66-340.
Institute and by
of the