NeuroscienceandBiobehavioralReviews,Vol. 16, pp. 371-378, 1992

0149-7634/92 $5.00 + .00 Copyright©1992PergamonPress Ltd.

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Perinatal Development of Human Circadian Rhythms: Role of the Foetal Biological Clock M. MIRMIRAN*,

J. H . K O K ~ , K. BOER:I: a n d H . WOLF:[:

*Netherlands Institute f or Brain Research, Amsterdam, The Netherlands t Department o f Neonatology and ~Department o f Obstetrics and Gynaecology, Academic Medical Centre, University o f Amsterdam, The Netherlands 17 S e p t e m b e r 1991 MIRMIRAN, M., J. H. KOK , K. BOER AND H. WOLF. Perinatal development of human circadian rhythms: role of thefoetal biologicalclock. NEUROSCI BIOBEHAV REV 16(3) 371-378, 1992. - T h e development of circadian rhythms and the neuronal mechanisms underlying their generation (particularly the suprachiasmatic nucleus of the hypothalamus) were reviewed. Based on perinatal animal studies and data from human foetuses and/or preterm infants it was concluded that human circadian rhythms are present as early as at 30 weeks of gestation. The significance of the mother and/or the environment regarding the entrainment of the "endogenous" foetal biological clock was emphasized. Circadian rhythms Human neonates

Suprachiasmatic nucleus

Pregnant women

CIRCADIAN rhythms are a common feature of all living systems (45, 70). Physiological phenomena such as sleepwakefulness, body temperature, release of different hormones, and activity of different brain neurotransmitters all exhibit circadian rhythms (10, 64, 66, 102). Although different areas of the brain may be able to generate circadian rhythms, a "biological clock" in the anterior hypothalamus, i.e., the suprachiasmatic nucleus (SCN), harmonizes these rhythms to induce a single circadian oscillation in mammals (38, 64, 82, 83). Circadian rhythms are endogenous, i.e., they are generated in the absence of any environmental time cues (the socalled "constant condition"). However, under natural conditions they are entrained to environmental light:dark cycles (in addition to social cues), and they are temporally interrelated; this "entrainment" and "internal synchronization" are aspects of the circadian rhythm-generating system, which appears to be important for the optimal functioning of the organism (85, 86, 110).

Human foetuses

Premature babies

levels of VP and VIP, as well as immunocytochemicai staining of both VP and VIP in the SCN during the light vs. dark phase of the 24-hour cycle show circadian rhythms in the SCN (3, I I , 31, 37, 51, 62, 63, 67, 80, 94, 108). (b) Daily electrical stimulation of the SCN mimics the effect of daily light exposure in the entrainment of circadian rhythms (84). (c) The hypothalamic island, including the SCN in situ, continues to show circadian rhythmicity, whereas areas outside the island do not (44). (d) Infusion of TTX (which block neuronal action potentials) into the SCN disrupts circadian rhythms. However, interestingly, upon TTX-withdrawal the phase of the recovered circadian rhythm corresponds with the original rhythm before drug delivery, as if the information about periodicity remained intact (intercellularly) within the SCN neurons even in the absence of extracellular neuronal activity during TTX exposure (88, 89). (e) Complete lesioning of the SCN eliminates the circadian rhythms of all physiological variables studied so far, including sleep-wake and body temperature (33, 36, 62, 85, 115). (f) Transplantation of foetal SCN in SCN-lesioned arythmic animals reestablishes circadian rhythms (25, 32, 50, 81, 96). Upon transplantation of the SCN, the period length of the circadian rhythms is determined by the donor SCN and not by the original rhythm (72). Furthermore, it was shown that rat SCN taken on embryonic day 12-16 (around the period in which these neurons are born) develops and differentiates normally when transplanted in oculo (79). This indicates that the phenotypic specification for SCN exists prior to the date of birth of its component neurons.

SCN AS A NEURONAL OSCILLATOR The hypothesis that the mammalian SCN neurons are able to generate circadian rhythms and sustain these in the absence of any external input is supported by the following lines of evidence: (a) Spontaneous electrical discharges of SCN neurons, SCN deoxyglucose uptake, release of neuropeptides synthesized in this nucleus [vasopressin (VP) and vasointestinal polypeptide (VIP)] in the cerebrospinal fluid (CSF), mRNA 371

372

M I R M I R A N , KOK, B O E R A N D W O L F FOETAL BIOLOGICAL CLOCK

SCN pacemaker neurons appear early in development. In an altricial mammal such as the rat, SCN neurons are formed from day 13-18 of gestation (4, 5, 19, 39, 49). An anatomically homologous SCN in the human hypothalamus has also been detected in the foetus (35, 52, 65, 99-101). One of the brain areas with a very high receptor density for pineal melatonin is the SCN. Using specific melatonin receptor ligands, Reppert and colleagues were able to show the human SCN in foetuses of 18-20 weeks of gestation (73). Recent evidence showing disruption of human circadian rhythms following a discrete hypothalamic lesion in the region of the SCN supports the hypothesis that the SCN serves as a neuronal oscillator underlying the generation of circadian rhythms, even in human [(17, 92); see also (18) for further support]. FOETAL CIRCADIAN RHYTHMS: ANIMAL STUDIES The first evidence suggesting that the foetal biological clock may be functional and entrainable by the mother came from a study by Deguchi (28). N-acetyltransferase (NAT) controls the melatonin production of the pineal gland. The SCN is responsible for the generation of the endogenous circadian rhythm of N A T activity (47). Deguchi has shown that rat pups born and raised under constant environmental conditions (constant light or constant darkness) show a clear circadian rhythmicity of N A T , independent of the environmental light and in phase with the original circadian rhythm o f the mother. He concluded that in the absence of the light:dark cycles, the mother sets the rhythm of the pup in order to synchronize it with her own. Furthermore, by having pups raised by foster mothers, he clearly showed that the original mother (prenatally) plays the dominant role in setting the phase of the foetal clock. Both Davis and Reppert have clearly established the prominent role of maternal SCN in setting the circadian rhythms of hamster and rat pups (20, 76, ll3). In a series of experiments, using the deoxyglucose method, Reppert and Schwartz demonstrated the presence of an active foetal biological clock, both in rat and monkey (74, 75). They showed clear day-night rhythms in the activity of the foetal SCN, which

was present in both rats and in monkeys. The activity o f the SCN neurons is higher during the light than during the dark, both in diurnal and nocturnal mammals [(87, 90); for review see (56)]. Recording spontaneous electrical discharges o f rat SCN neurons has shown that, as early as the last day o f gestation, a circadian rhythm can be observed in the activity of this nucleus (93). This rhythm remains intact even if the nucleus is cultured for several weeks in vitro (11). Dispersed cell suspension of the foetal hamster SCN containing VP neurons on embryonic day 14 can restore the circadian rhythms of arrhythmic animals (96). In pregnant monkeys, oestriol, progesterone, and dehydroepiandrostrone sulphate, which are believed to be mainly products of the foetal adrenal, show a clear circadian rhythm, with a peak at night in phase with the peak of the maternal uterine activity rhythm (112). A clear synchronization between the activity of the maternal and foetal biological clocks has been shown in lamb studies. It is known that the circadian rhythm of vasopressin (AVP) in the CSF is the function of the rhythmic activity of the SCN (91). Stark and Daniel (98) have shown a clear synchronization between the phase of the circadian rhythm of A V P in the CSF of the pregnant ewe and foetal lamb during the last trimester of gestation. Interestingly, they have also shown that keeping pregnant ewes under a constant light condition eliminates both the maternal and foetal A V P rhythms. In all, these animal studies suggest perinatal emergence of circadian rhythms with active participation of the foetal biological clock. FOETAL CIRCADIAN RHYTHMS: HUMAN STUDIES Many overt rhythms driven by the biological clock have been shown to be present during human prenatal life [for review see (43, 58)] (Table 1). There is a circadian rhythm of rest-activity and heart rate in the foetus (6, 13, 26, 68, 109, 111). It is not easy to monitor foetal rhythms under natural conditions for several days to allow meaningful measures of circadian rhythms. Using a small ambulatory monitor, which we developed ourselves (57), for recording both maternal restactivity and body temperature, we were able to record for the first time over a period of one week the circadian rhythms

TABLE l DATA OF 12 "HEALTHY" PRETERM INFANTS RECORDED FOR A SUFFICIENT PERIOD OF TIME TO BE ABLE TO ANALYZE FOR PRESENCE/ABSENCE OF CIRCADIAN RHYTHMS (61). CIRCADIAN RHYTHMS WERE PRESENT IN THE BODY TEMPERATURE AND HEART RATE OF ABOUT 50% OF THESE INFANTS Name

GestationalAge

BIH JIB QUT TIH ARG JOB SAG CHF ARB IRZ ESA LED

25 26 26 26 28 28 28 29 30 31 32 32

girl girl girl boy boy boy boy girl boy girl girl boy

Conceptional Age

Apgar5 min

RecordingDays

M

T

H

33 30 29 29 32 31 31 33 35 33 34 34

9 9 l0 9 l0 8 l0 8 7 9 9 9

14 8 8 14 14 l0 7 12 4 10 8 13

--

*

*

*

*

*

-

*

* *

---

* * * *

* -

*Statistically significant circadian periodicity was present. Motility (M), body temperature (T), heart rate (H).

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FIG. 1. The rest-activity and body temperature of a 33-week pregnant woman recorded continuously over a period of more than 1 week are displayed on the lefthand side. On the right, the chi-square periodgrams are shown [see also (57)], indicating a significant circadian periodicity with a 24-hour peak period length for both physiological variables.

of these physiological variables in six pregnant women during the last trimester of gestation under natural living conditions (Fig. 1). These rhythms were fully entrained to the 24 h zeitgebers. The foetal heart rate rhythm has been found as early as at 22 weeks of gestation (26). It is important to know whether the foetal rhythms recorded during human gestation simply reflect the influence of a maternal circadian system or whether the foetal biological clock also plays an important mediatory role. If the latter is true, the biological clock of the foetus itself, independent of that of the mother, ought to be able to generate a certain level of circadian rhythmicity. Since it is obviously impossible to record foetal circadian rhythms in the absence of maternal influences, we have carried out a study in which the circadian rhythms of body temperature, heart rate, and rest-activity cycles of preterm infants were recorded. Two series of studies were carried out. The first includes continuous recordings for several days (59), while in the second series of experiments we recorded preterm infants over a period of 1-2 weeks [(60, 61); see Fig. 2]. We were indeed able to demonstrate circadian rhythms in certain physiological variables, such as body temperature (and to a lesser extent heart rate), of 50% of the preterm infants at the conceptual age of 29-35 weeks in both studies (59-61). However, the period lengths of these rhythms varied from day to day. Thus, the rhythms were not entrained to the time of day. And, as has been shown in Table 1, only in one infant (see Fig. 2) was a circadian rhythm of rest-activity present. Similar early development was also found for body temperature and corticosterone in other studies (1, 97). Figure 3 illustrates the circadian rhythm of body temperature of a 33-week-old preterm infant recorded inside the incubator under a constant environmental temperature, constant light and an every two hours

feeding schedule. For comparison, the circadian rhythm of the body temperature of a pregnant woman recorded at 33 weeks of gestation is also shown. Although it is clear that the circadian rhythm of the mother (and thus of the foetus under her influence) is much more profound than that of the infant, the biological clock of the premature infant is nevertheless independent of maternal influences and able to generate circadian rhythms. It is important to realize that the pregnant woman is entrained to the 24 h zeitgebers, while preterm infants in the incubator live under a rather constant condition (so-called constant routine). It is well known from studies in adults that such a condition reduces the amplitude of the circadian rhythms and may lead to internal desynchronization. This emphasizes the importance of introducing zeitgebers to the neonatal intensive care unit to ensure a better development of the circadian rhythms of preterm infants (see below). PATHWAYS THE FOETAL

FOR ENTRAINING BIOLOGICAL CLOCK

Animal studies have demonstrated that an intact maternal SCN is a necessary factor for the mother-foetus entrainment of prenatal circadian rhythms (20, 21, 76, 78). Total lesion of the maternal SCN on gestational day 7 diminished both the circadian rhythmicity of deoxyglucose uptake in the foetal SCN, as well as the rhythm of pineal NAT activity in 10-dayold pups. Still, rhythmicity in individual rat foetuses and pups is thought to persist despite maternal SCN lesion. The phase of rhythmicity of the individuals is, however, uncoordinated due to the absence of a maternal entraining signal (20, 76). The later postnatal appearance of both free-running and entrainment of circadian rhythms seems to develop normally in

374

MIRMIRAN, KOK, BOER AND W O L F

rats and mice subjected to disturbances of maternal circadian rhythms during the perinatal period (20, 22, 76). An in vitro deoxyglucose uptake study (95), in which either the SCN or the rest of the anterior hypothalamus was taken from rat foetuses of intact mothers, of mothers with total SCN lesions reared under light:dark conditions or of intact mothers living under constant light conditions demonstrated that (a) the foetal SCN deoxyglucose activity (and not the rest of the hypothalamic area) shows a circadian rhythm and (b) both constant light and SCN lesion, known to disrupt the maternal circadian rhythm, diminish the SCN rhythm of the foetus (54, 95). There are many ways in which maternal circadian rhythms (generated by the SCN of the mother) may entrain and potentiate human foetal circadian rhythms. These include: corticosterone releasing factor (CRF), cortisol, melatonin, glucose availability, body temperature, and uterine contractures. Patrick and colleagues have suggested that in humans the maternal glucocorticoids may influence foetal adrenal function, thereby entraining the circadian rhythms of the foetus [(69); for a review see (24, 43)]. The circadian rhythm of maternal CRF and cortisol may influence foetal SCN activity through a high amount of glucorticosteroid receptors particularly present in this nucleus during early development (27). There is strong evidence in favor of the maternal cortisol rhythm being

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involved in the regulation of human foetal circadian rhythms. It has been well demonstrated that blocking maternal cortisol with triamcinolone or total maternal adrenalectomy (with continuous cortisol supplementation) may eliminate the circadian rhythms of heart rate, breathing, and motility of the human foetus (7, 8). Via its influence on the circadian rhythm of maternal uterine activity, corticosterone may also influence foetal rhythms (29). Melatonin is a potent factor in inhibiting SCN activity, which is able to entrain circadian rhythms (9, 15, 16, 107). The circadian rhythm of maternal melatonin (which easily passes through the placenta as well as the blood-brain barrier) may entrain the activity of the foetal SCN to be in phase with that of the maternal SCN. Prenatal entrainment of the foetal SCN pacemaker has indeed been shown in rodents by daily administration of melatonin to the mother (23). Melatonin can indeed entrain the circadian rhythms of the pups of SCNlesioned arrhythmic mothers (23). However, animal studies have demonstrated that most of the endocrine organs are not very crucial for entrainment of foetal circadian rhythms and yet, the maternal SCN plays a key role [(77), but see also (48)]. The circadian rhythm of body temperature constitutes another manner in which the maternal SCN may entrain the foetal clock. The role of the SCN in glucose regulation and the circadian rhythmicity of glucose availability (116) can also be considered mediatory factors in the transmission of the maternal rhythm to the foetus. It is interesting that periodic feeding of SCN-lesioned dams can entrain foetal and infant rats (41, 42, 103, 104, 114). The rhythmic circadian variation of uterine contractures present throughout the last trimester of gestation is a potent tactile stimulus which, by changing the behavioral states of the foetus, influences its circadian rhythmicity (29, 105). As Nathanielsz puts it, "that's how the mother talks with her fetus." All in all, there are many ways in which the mother, directly or indirectly, influences the foetal biological clock and potentiates and entrains the circadian rhythms of an entrainable foetus. Although it is known that the maternal biological clock is a necessary factor, it is yet to be established whether there is a direct link between the maternal and foetal SCN or if the different circadian rhythms of the mother ("hands of the clock") influence the foetal hypothalamus. What should be considered, given the results of this review, is the fact that the foetal biological clock plays an active role in the generation of prenatal circadian rhythms. FUNCTIONAL SIGNIFICANCE OF PRENATAL CIRCADIAN RHYTHMS

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FIG. 2. Circadian rhythms of heart rate, body temperature, and restactivity cycles of a preterm infant recorded inside an incubator under continuous light and constant ambient temperature and intragastric feeding every 2 hours in the neonatal intensive care unit [see also (5961)].

An important function of maternal entrainment during the perinatal development may be preparing the offspring circadian time-keeping system for later independent life (20, 30, 78). Maternal rhythm disturbances during gestation diminish the circadian rhythmicity of the foetal clock (12, 94, 98). Lesioning of the maternal SCN disrupts the phase of entrainment of the drinking activity rhythm at weaning in rat/hamster pups born from and raised by SCN-lesioned mothers (20, 21, 76, 78). However, individual animal rhythms persist later in life due to the intact SCN of the offspring. The circadian rhythm of NAT, which is one of the first overt rhythms to be detected in postnatal life, is not present in intact pups born of and raised by SCN-lesioned mothers (76). To demonstrate the relative contribution of pre- and early postnatal life, geppert and Schwartz let pups born of SCN-lesioned mothers be raised by intact, lactating mothers and vice versa. Only the prenatally lesioned group showed a clearly disturbed NAT rhythm. It is believed that entrainment of the foetal biological clock by the

P E R I N A T A L H U M A N C I R C A D I A N RHYTHM

375

BODY TEMPERATURE (°C)

PERIODOGRAM

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,,111,,,,,

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PERIOD LENGTH (HOUR)

FIG. 3. Comparison between the circadian rhythm of body temperature of a 33-week pregnant woman (top left) and that of a preterm infant with a conceptional age of 33 weeks (bottom left). The corresponding chi-square periodgrams show a significant circadian rhythm with a period length of 24 h in both subjects.

maternal SCN may occur in rats from day 10 of gestation until day 5 of postnatal life [(30, 41,42, 74, 76, 103); see also (71)]. The functional significance of human maternal entrainment for the development of the circadian system of the child is not yet known. It is probable though, that the postnatal development of human circadian rhythms may be affected by disturbances during perinatal life. This possibility is exemplified by what happens when the intimate mother-foetus relationship is broken off prematurely. It has often been observed that sleep problems are more common in pre- than in full-term infants (40, 46, 53, 55,106). Preterm infants stay in the neonatal intensive care unit under a constant light illumination and temperature. They therefore miss several important maternal entraining factors, such as the circadian rhythms of CRF, cortisol, melatonin, and uterine contractures, in addition to maternally mediated day-night information. In our studies on the development of circadian rhythms (59-61), we found a circadian rhythm of body temperature in 50°70 of the preterm infants we examined, some as young as 29 weeks of conceptional age. These rhythms were not in accordance with the time of the day in successive recording days, and their period lengths varied from day to day (Figs. 2 and 3). However, if these infants had not been born prematurely, they would have had stable circadian rhythms synchronized with the time of day by the influence of the maternally mediated stable daynight cycle (see Figs. 1 and 3). From our data, we can conclude that although a human biological clock capable of generating certain circadian rhythms is present as early as at 29 weeks of gestation, the maternal circadian rhythms are most probably important for the optimal functioning of this endogenous clock. It has been shown in experimental studies that an en-

dogenous biological clock capable of generating circadian rhythms will continue oscillating more optimally if kept under an oscillating rhythmic environment. However, the amplitude, period length, and interdaily stability of the rhythm will become variable in a constant non-oscillating environment (2, 11, 31, 45, 54, 98, 102). Future research is required in which the lack of prenatal maternal factors necessary for the proper development of the foetal biological clock should be compensated for by raising preterm infants in light:dark conditions (instead of the continuous light condition of the intensive care unit). Recent studies in which the development of preterm infants in intensive care units exposed to a light:dark rhythm was compared with the development of those exposed to continuous light have indicated a clear advantage for the earlier group [(34, 53); see also (55)1. The very recent study by McMillen, Kok, Adamson, Deayton, and Nowak comparing the development of light:dark entrainment in preterm and fullterm infants is of great interest in this respect. The results of this study indicate, first of all, that preterm infants as young as 35 weeks of conceptional age are entrainable to environmental time cues, secondly, it shows that a longer duration of exposure to the cyclic environment (including light:dark cycle and periodic maternal care) leads to an earlier development of entrainment in these infants (55). ACKNOWLEDGEMENTS We are grateful to the pregnant women and the mothers of preterm infants for their enthusiasm and cooperation regarding our ongoing studies on perinatal development of circadian rhythms, partly presented in this review. Olga Pach did most of the time-consuming editing of this manuscript.

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M I R M I R A N , KOK, B O E R A N D W O L F REFERENCES

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PERINATAL

44. 45. 46. 47.

48. 49. 50.

51. 52. 53. 54. 55. 56. 57. 58.

59. 60. 61. 62. 63. 64. 65. 66.

HUMAN

CIRCADIAN

RHYTHM

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Perinatal development of human circadian rhythms: role of the foetal biological clock.

The development of circadian rhythms and the neuronal mechanisms underlying their generation (particularly the suprachiasmatic nucleus of the hypothal...
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