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Maternal neglect and the serotonin system are associated with daytime sleep in infant rhesus monkeys

Published online by Cambridge University Press:  04 February 2019

Alexander Baxter Open the ORCID record for Alexander Baxter [Opens in a new window] ,
Elizabeth K. Wood Open the ORCID record for Elizabeth K. Wood [Opens in a new window] ,
Christina S. Barr ,
Daniel B. Kay ,
Stephen J. Suomi  and
J. Dee Higley
Alexander Baxter
Affiliation:
Department of Psychology, Brigham Young University, Provo, UT, USA
Elizabeth K. Wood
Affiliation:
Department of Psychology, Brigham Young University, Provo, UT, USA
Christina S. Barr
Affiliation:
Section of Comparative Behavioral Genomics, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health Rockville, MD, USA
Daniel B. Kay
Affiliation:
Department of Psychology, Brigham Young University, Provo, UT, USA
Stephen J. Suomi
Affiliation:
Laboratory of Comparative Ethology, National Institute of Child Health and Human Development, National Institutes of Health, Poolesville, MD, USA
J. Dee Higley*
Affiliation:
Department of Psychology, Brigham Young University, Provo, UT, USA
*
Address for Correspondence: J. Dee Higley, Department of Psychology, 1042 KMBL, Brigham Young University, Provo, UT84602. E-mail: [email protected].
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Abstract

Environmental and biological factors contribute to sleep development during infancy. Parenting plays a particularly important role in modulating infant sleep, potentially via the serotonin system, which is itself involved in regulating infant sleep. We hypothesized that maternal neglect and serotonin system dysregulation would be associated with daytime sleep in infant rhesus monkeys. Subjects were nursery-reared infant rhesus macaques (n = 287). During the first month of life, daytime sleep-wake states were rated bihourly (0800–2100). Infants were considered neglected (n = 16) if before nursery-rearing, their mother repeatedly failed to retrieve them. Serotonin transporter genotype and concentrations of cerebrospinal fluid 5-hydroxyindoleacetic acid (5-HIAA) were used as markers of central serotonin system functioning. t tests showed that neglected infants were observed sleeping less frequently, weighed less, and had higher 5-HIAA than non-neglected nursery-reared infants. Regression revealed that serotonin transporter genotype moderated the relationship between 5-HIAA and daytime sleep: in subjects possessing the Ls genotype, there was a positive correlation between 5-HIAA and daytime sleep, whereas in subjects possessing the LL genotype there was no association. These results highlight the pivotal roles that parents and the serotonin system play in sleep development. Daytime sleep alterations observed in neglected infants may partially derive from serotonin system dysregulation.

Keywords

development5-hydroxyindoleacetic acidinfant sleepmaternal neglectserotonin transporter gene
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 1 , February 2020 , pp. 1 - 10
Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

A.B. and E.K.W. are equal contributors.

†

D.B.K., S.J.S., and J.D.H. are equal contributors.

References

Ball, H. L. (2003). Breastfeeding, bed-sharing, and infant sleep. Birth, 30, 181–188.CrossRefGoogle ScholarPubMed
Barclay, N. L., Eley, T. C., Mill, J., Wong, C. C. Y., Zavos, H. M. S., Archer, S. N., & Gregory, A. M. (2011). Sleep quality and diurnal preference in a sample of young adults: Associations with 5HTTLPR, PER3, and CLOCK 3111. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 156 B, 681–690. doi:10.1002/ajmg.b.31210CrossRefGoogle Scholar
Barkovich, A., Kjos, B., Jackson, D., & Norman, D. (1988). Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology, 166, 173–180.CrossRefGoogle ScholarPubMed
Barrett, C. E., Noble, P., Hanson, E., Pine, D. S., Winslow, J. T., & Nelson, E. E. (2009). Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol levels in juvenile rhesus monkeys. Psychoneuroendocrinology, 34, 1029–1040. doi:10.1016/j.psyneuen.2009.02.002CrossRefGoogle ScholarPubMed
Bathory, E., & Tomopoulos, S. (2017). Sleep regulation, physiology and development, sleep duration and patterns, and sleep hygiene in infants, toddlers, and preschool-age children. Current Problems in Pediatric and Adolescent Health Care, 47, 29–42. doi:10.1016/j.cppeds.2016.12.001CrossRefGoogle ScholarPubMed
Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746–754.CrossRefGoogle ScholarPubMed
Bennett, A. J., Lesch, K. P., Heils, A., Long, J. C., Lorenz, J. G., Shoaf, S. E., … Higley, J. (2002). Early experience and serotonin transporter gene variation interact to influence primate CNS function. Molecular Psychiatry, 7, 118.CrossRefGoogle ScholarPubMed
Biagioni, E., Boldrini, A., Giganti, F., Guzzetta, A., Salzarulo, P., & Cioni, G. (2005). Distribution of sleep and wakefulness EEG patterns in 24-h recordings of preterm and full-term newborns. Early Human Development, 81, 333–339.CrossRefGoogle ScholarPubMed
Bowman, R. E., Wolf, R. C., & Sackett, G. P. (1970). Circadian rhythms of plasma 17-hydroxycorticosteroids in the infant monkey. Proceedings of the Society for Experimental Biology and Medicine, 133, 342–344.CrossRefGoogle ScholarPubMed
Brummett, B. H., Krystal, A. D., Ashley-Koch, A., Kuhn, C. M., Züchner, S., Siegler, I. C., … Williams, R. B. (2007). Sleep quality varies as a function of 5-HTTLPR genotype and stress. Psychosomatic Medicine, 69, 621.CrossRefGoogle Scholar
Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry, 167, 509–527.CrossRefGoogle ScholarPubMed
Champoux, M., & Suomi, S. J. (1988). Behavioral development of nursery-reared rhesus macaque (Macaca mulatta) neonates. Infant Behavior and Development, 11, 363–367.CrossRefGoogle Scholar
Cohen-Mansfield, J., Waldhorn, R., Werner, P., & Billig, N. (1990). Validation of sleep observations in a nursing home. Sleep, 13, 512–525.CrossRefGoogle Scholar
Daws, L. C., & Gould, G. G. (2011). Ontogeny and regulation of the serotonin transporter: Providing insights into human disorders. Pharmacology and Therapeutics, 131, 61–79. doi:10.1016/j.pharmthera.2011.03.013CrossRefGoogle ScholarPubMed
Deley, J. T., Turner, R. S., Freeman, A., Bliwise, D. L., & Rye, D. B. (2006). Prolonged assessment of sleep and daytime sleepiness in unrestrained Macaca mulatta. Sleep, 29, 221–231.Google Scholar
Deuschle, M., Schredl, M., Schilling, C., Wüst, S., Frank, J., Witt, S. H., … Schulze, T. G. (2010). Association between a serotonin transporter length polymorphism and primary insomnia. Sleep, 33, 343–347.CrossRefGoogle ScholarPubMed
Dewey, K. G. (1998). Growth characteristics of breast-fed compared to formula-fed infants. Neonatology, 74, 94–105.CrossRefGoogle ScholarPubMed
Ednick, M., Cohen, A., McPhail, G., Beebe, D., & Simakajornboon, N. (2009). A review of the effects of sleep during the first year of life on cognitive, psychomotor, and temperament development. Sleep, 32, 1449–1458.CrossRefGoogle ScholarPubMed
Emde, R. N., Harmon, R. J., Metcalf, D., Koenig, K. L., & Wagonfeld, S. (1971). Stress and neonatal sleep. Psychosomatic Medicine, 33, 491–497. doi:10.1097/00006842-197111000-00002CrossRefGoogle ScholarPubMed
Fagioli, I., & Salzarulo, P. (1982). Sleep states development in the first year of life assessed through 24-h recordings. Early Human Development, 6, 215–228. doi:https://doi.org/10.1016/0378-3782(82)90109-8CrossRefGoogle ScholarPubMed
Figueiredo, B., Dias, C. C., Pinto, T. M., & Field, T. (2016). Infant sleep-wake behaviors at two weeks, three and six months. Infant Behavior and Development, 44, 169–178. doi:http://dx.doi.org/10.1016/j.infbeh.2016.06.011CrossRefGoogle ScholarPubMed
Filonzi, L., Magnani, C., Nosetti, L., Nespoli, L., Borghi, C., Vaghi, M., & Marzano, F. N. (2012). Serotonin transporter role in identifying similarities between SIDS and idiopathic ALTE. Pediatrics, 130(e138–e144.CrossRefGoogle ScholarPubMed
Fisher, L., Ames, E. W., Chisholm, K., & Savoie, L. (1997). Problems reported by parents of Romanian orphans adopted to British Columbia. International Journal of Behavioral Development, 20, 67–82. doi:10.1080/016502597385441CrossRefGoogle Scholar
Gibbs, R. A., Rogers, J., Katze, M. G., Bumgarner, R., Weinstock, G. M., Mardis, E. R., … Wilson, R. K. (2007). Evolutionary and biomedical insights from the rhesus macaque genome. Science, 316, 222–234.Google ScholarPubMed
Graven, S. N., & Browne, J. V. (2008). Sleep and brain development: The critical role of sleep in fetal and early neonatal brain development. Newborn and Infant Nursing Reviews, 8, 173–179.CrossRefGoogle Scholar
Gregory, A. M., Caspi, A., Eley, T. C., Moffitt, T. E., O'connor, T. G., & Poulton, R. (2005). Prospective longitudinal associations between persistent sleep problems in childhood and anxiety and depression disorders in adulthood. Journal of Abnormal Child Psychology, 33, 157–163.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Malone, S., Vance, G., & Fisch, R. O. (1985). Coping with aversive stimulation in the neonatal period: Quiet sleep and plasma cortisol levels during recovery from circumcision. Child Development, 56, 824–834. doi:10.2307/1130094CrossRefGoogle ScholarPubMed
Harlow, H. (1958). The nature of love. American Psychologist, 13, 673.CrossRefGoogle Scholar
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Publications.Google Scholar
Heils, A., Teufel, A., Petri, S., Stober, G., Riederer, P., Bengel, D., & Lesch, K. P. (1996). Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry, 66, 2621–2624.CrossRefGoogle ScholarPubMed
Higley, J. D., Bennett, A. J., Helis, A., Lesch, K. P., Shoaf, S. E., White, I. M., … Linnoila, M. (1998). Serotonin transporter gene variation is associated with CSF 5-HIAA concentrations in rhesus monkeys. Society for Neuroscience Abstracts, 24, 1113.Google Scholar
Hinde, R. A., & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour, 15, 169–196. doi:https://doi.org/10.1016/S0003-3472(67)80029-0CrossRefGoogle ScholarPubMed
Hofer, M. A. (1983). The mother-infant interaction as a regulator of infant physiology and behavior. In Rosenblum, L. (Ed.), Symbiosis in parent-offspring interactions (pp. 61–75). Springer, Boston, MA.CrossRefGoogle Scholar
Huang, Y.-S., Paiva, T., Hsu, J.-F., Kuo, M.-C., & Guilleminault, C. (2014). Sleep and breathing in premature infants at 6 months post-natal age. BMC Pediatrics, 14, 303. doi:10.1186/s12887-014-0303-6CrossRefGoogle ScholarPubMed
Iwata, S., Fujita, F., Kinoshita, M., Unno, M., Horinouchi, T., Morokuma, S., & Iwata, O. (2017). Dependence of nighttime sleep duration in one-month-old infants on alterations in natural and artificial photoperiod. Scientific Reports, 7, 44749.CrossRefGoogle ScholarPubMed
Jones, B. E. (2003). Arousal systems. Frontiers in Bioscience, 8, s438–s451.CrossRefGoogle ScholarPubMed
Jouvet, M. (1999). Sleep and serotonin: An unfinished story. Neuropsychopharmacology, 21, 24S–27S.Google Scholar
Kaemingk, K., & Reite, M. (1987). Social environment and nocturnal sleep: Studies in peer-reared monkeys. Sleep, 10, 542–550.CrossRefGoogle ScholarPubMed
Kelleher, S. L., Chatterton, D., Nielsen, K., & Lönnerdal, B. (2003). Glycomacropeptide and α-lactalbumin supplementation of infant formula affects growth and nutritional status in infant rhesus monkeys. The American Journal of Clinical Nutrition, 77, 1261–1268.CrossRefGoogle ScholarPubMed
Kepser, L.-J., & Homberg, J. R. (2015). The neurodevelopmental effects of serotonin: A behavioural perspective. Behavioural Brain Research, 277, 3–13.CrossRefGoogle ScholarPubMed
Knobel, R. B. (2014). Fetal and neonatal thermal physiology. Newborn and Infant Nursing Reviews, 14, 45–49.CrossRefGoogle Scholar
Koga, A., Fukushima, A., Sakuma, K., & Kagawa, Y. (2016). Association between sleep duration and personality-gene variants: Sleep duration is longer in S/S homozygotes of serotonin transporter than in L allele genotypes. Journal of Sleep Disorders: Treatment and Care, 4.Google Scholar
Kohyama, J. (1998). Sleep as a window on the developing brain. Current Problems in Pediatrics, 28, 73–92. doi:https://doi.org/10.1016/S0045-9380(98)80054-6CrossRefGoogle ScholarPubMed
Lam, P., Hiscock, H., & Wake, M. (2003). Outcomes of infant sleep problems: A longitudinal study of sleep, behavior, and maternal well-being. Pediatrics, 111, e203–e207.CrossRefGoogle ScholarPubMed
Lavezzi, A. M., Casale, V., Oneda, R., Weese-Mayer, D. E., & Matturri, L. (2009). Sudden infant death syndrome and sudden intrauterine unexplained death: Correlation between hypoplasia of raphe nuclei and serotonin transporter gene promoter polymorphism. Pediatric Research, 66, 22–27. doi:10.1203/PDR.0b013e3181a7bb73CrossRefGoogle ScholarPubMed
Lesch, K.-P., Balling, U., Gross, J., Strauss, K., Wolozin, B. L., Murphy, D. L., & Riederer, P. (1994). Organization of the human serotonin transporter gene. Journal of Neural Transmission General Section, 95, 157–162.CrossRefGoogle ScholarPubMed
Lubach, G. R., & Coe, C. L. (2006). Immunological consequences of nursery rearing. In Sackett, G. P., Ruppenthal, G., & Elias, K. (Eds.), Nursery rearing of nonhuman primates in the 21st century (pp. 135–168). New York, NY: Springer.CrossRefGoogle Scholar
Lubach, G. R., Kittrell, E. M. W., & Coe, C. L. (1992). Maternal influences on body temperature in the infant primate. Physiology & Behavior, 51, 987–994.CrossRefGoogle ScholarPubMed
Maestripieri, D., Higley, J. D., Lindell, S. G., Newman, T. K., McCormack, K. M., & Sanchez, M. M. (2006). Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behavioral Neuroscience, 120, 1017–1024. doi:10.1037/0735-7044.120.5.1017CrossRefGoogle Scholar
McCall, E. M., Alderdice, F. A., Halliday, H. L., Jenkins, J. G., & Vohra, S. (2006). Interventions to prevent hypothermia at birth in preterm and/or low birthweight babies. Evidence-Based Child Health: A Cochrane Review Journal, 1, 287–324.CrossRefGoogle Scholar
McCormack, K., Howell, B., Guzman, D., Villongco, C., Pears, K., Kim, H., … Sanchez, M. (2015). The development of an instrument to measure global dimensions of maternal care in rhesus macaques (Macaca mulatta). American Journal of Primatology, 77, 20–33.CrossRefGoogle Scholar
McGraw, K., Hoffmann, R., Harker, C., & Herman, J. H. (1999). The development of circadian rhythms in a human infant. Sleep, 22, 303–310.CrossRefGoogle Scholar
Mehlman, P. T., Westergaard, G. C., Hoos, B. J., Sallee, F. R., Marsh, S., Suomi, S. J., … Higley, J. D. (2000). CSF5-HIAA and nighttime activity in free-ranging primates. Neuropsychopharmacology, 22, 210–218. doi:10.1016/s0893-133x(99)00101-3CrossRefGoogle Scholar
Meier, G. W., & Berger, R. J. (1965). Development of sleep and wakefulness patterns in the infant rhesus monkey. Experimental Neurology, 12, 257–277.CrossRefGoogle ScholarPubMed
Monti, J. M., & Jantos, H. (2008). The roles of dopamine and serotonin, and of their receptors, in regulating sleep and waking. Progress in Brain Research, 172, 625–646. doi:10.1016/S0079-6123(08)00929-1CrossRefGoogle ScholarPubMed
Moss, H. A. (1967). Sex, age, and state as determinants of mother-infant interaction. Merrill-Palmer Quarterly of Behavior and Development, 13, 19–36.Google Scholar
Olivier, J. D., Åkerud, H., Kaihola, H., Pawluski, J. L., Skalkidou, A., Högberg, U., & Sundström-Poromaa, I. (2013). The effects of maternal depression and maternal selective serotonin reuptake inhibitor exposure on offspring. Frontiers in Cellular Neuroscience, 7, 1–15.CrossRefGoogle ScholarPubMed
Ong, S. H., Wickramaratne, P., Tang, M., & Weissman, M. M. (2006). Early childhood sleep and eating problems as predictors of adolescent and adult mood and anxiety disorders. Journal of Affective Disorders, 96, 1–8.CrossRefGoogle ScholarPubMed
Papailiou, A., Sullivan, E., & Cameron, J. L. (2008). Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured by accelerometer. American Journal of Primatology, 70, 185–190. doi:10.1002/ajp.20476CrossRefGoogle ScholarPubMed
Parmelee, A. H., Wenner, W. H., & Schulz, H. R. (1964). Infant sleep patterns: From birth to 16 weeks of age. The Journal of Pediatrics, 65, 576–582.CrossRefGoogle ScholarPubMed
Reite, M., Rhodes, J., Kavan, E., & Adey, W. (1965). Normal sleep patterns in macaque monkey. Archives of Neurology, 12, 133–144.CrossRefGoogle ScholarPubMed
Reite, M., Short, R., Kaufman, I., Stynes, A., & Pauley, J. (1978). Heart rate and body temperature in separated monkey infants. Biological Psychiatry, 13, 91–105.Google ScholarPubMed
Rogers, J., Kaplan, J., Garcia Iv, R., Shelledy, W., Nair, S., & Cameron, J. (2006). Mapping of the serotonin transporter locus (SLC6A4) to rhesus chromosome 16 using genetic linkage. Cytogenetic and Genome Research, 112, 341A–341A.CrossRefGoogle ScholarPubMed
Sackett, G., Fahrenbruch, C., & Ruppenthal, G. (1979). Development of basic physiological parameters and sleep-wakefulness patterns in normal and at-risk neonatal pigtail macaques (Macaca nemestrina). In Ruppenthal, G. & Reese, D. (Eds.), Nursery care of nonhuman primates. Advances in primatology. (pp. 125–142). Boston, MA: Springer.CrossRefGoogle Scholar
Scaramuzzo, R. T., Giampietri, M., Fiorentini, E., Bartalena, L., Fiori, S., Guzzetta, A., … Ghirri, P. (2015). Serum cortisol concentrations during induced hypothermia for perinatal asphyxia are associated with neurological outcome in human infants. Stress: The International Journal on the Biology of Stress, 18, 129–133. doi:10.3109/10253890.2014.987120CrossRefGoogle ScholarPubMed
Scheinin, M., Chang, W.-H., Kirk, K. L., & Linnoila, M. (1983). Simultaneous determination of 3-methoxy-4-hydroxyphenylglycol, 5-hydroxyindoleacetic acid, and homovanillic acid in cerebrospinal fluid with high-performance liquid chromatography using electrochemical detection. Analytical Biochemistry, 131, 246–253.CrossRefGoogle ScholarPubMed
Scher, M. S., & Loparo, K. A. (2009). Neonatal EEG/sleep state analyses: A complex phenotype of developmental neural plasticity. Developmental Neuroscience, 31, 259–275.CrossRefGoogle ScholarPubMed
Seppala, T., Scheinin, M., Capone, A., & Linnoila, M. (1984). Liquid chromatographic assay for CSF catecholamines using electrochemical detection. Acta Pharmacologica et Toxicologica, 55, 81–87.CrossRefGoogle ScholarPubMed
Shannon, C., Champoux, M., & Suomi, S. J. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology, 46, 311–321.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Shannon, C., Schwandt, M. L., Champoux, M., Shoaf, S. E., Suomi, S. J., Linnoila, M., & Higley, J. D. (2005). Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants. American Journal of Psychiatry, 162, 1658–1664.CrossRefGoogle ScholarPubMed
Spinelli, S., Chefer, S., Suomi, S. J., Higley, J. D., Barr, C. S., & Stein, E. (2009). Early-life stress induces long-term morphologic changes in primate brain. Archives of General Psychiatry, 66, 658–665.CrossRefGoogle ScholarPubMed
Spruyt, K., Aitken, R. J., So, K., Charlton, M., Adamson, T. M., & Horne, R. S. C. (2008). Relationship between sleep/wake patterns, temperament and overall development in term infants over the first year of life. Early Human Development, 84, 289–296. doi:https://doi.org/10.1016/j.earlhumdev.2007.07.002CrossRefGoogle ScholarPubMed
Suomi, S. J. (2006). Risk, resilience, and gene × environment interactions in rhesus monkeys. Annals of the New York Academy of Sciences, 1094, 52–62.CrossRefGoogle ScholarPubMed
Vohr, B. R., Wright, L. L., Dusick, A. M., Mele, L., Verter, J., Steichen, J. J., … Bauer, C. R. (2000). Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993–1994. Pediatrics, 105, 1216–1226.CrossRefGoogle Scholar
Waldron, S., & MacKinnon, R. (2007). Neonatal thermoregulation. Infant, 3, 101–104.Google Scholar
Welberg, L. M., & Seckl, J. R. (2001). Prenatal stress, glucocorticoids and the programming of the brain. Journal Of Neuroendocrinology, 13, 113–128. doi:10.1046/j.1365-2826.2001.00601.xCrossRefGoogle Scholar
Williams, R. B., Marchuk, D. A., Gadde, K. M., Barefoot, J. C., Grichnik, K., Helms, M. J., … Siegler, I. C. (2003). Serotonin-related gene polymorphisms and central nervous system serotonin function. Neuropsychopharmacology, 28, 533–541. doi:10.1038/sj.npp.1300054CrossRefGoogle ScholarPubMed
Young, S. N., Gauthier, S., Anderson, G. M., & Purdy, W. C. (1980). Tryptophan, 5-hydroxyindoleacetic acid and indoleacetic acid in human cerebrospinal fluid: interrelationships and the influence of age, sex, epilepsy and anticonvulsant drugs. Journal of Neurology, Neurosurgery, and Psychiatry, 43, 438–445.CrossRefGoogle ScholarPubMed
Zajicek, K. B., Higley, J. D., Suomi, S. J., & Linnoila, M. (1997). Rhesus macaques with high CSF 5-HIAA concentrations exhibit early sleep onset. Psychiatry Research, 73, 15–25.CrossRefGoogle ScholarPubMed
Zeskind, P. S., & Stephens, L. E. (2004). Maternal selective serotonin reuptake inhibitor use during pregnancy and newborn neurobehavior. Pediatrics, 113, 368–375.CrossRefGoogle ScholarPubMed
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