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Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants
Open accessAbstract
A functional polymorphism in the promoter region of the serotonin transporter (5-HTTLPR) gene has been associated with variation in anxiety and hypothalamus-pituitary-adrenal (HPA) axis function in humans and rhesus macaques. Individuals carrying the short allele are at a higher risk for developmental psychopathology, and this risk is magnified in short allele carriers who have experienced early life stress. This study investigated the relationship between 5-HTTLPR allelic variation, infant abuse, and behavioral and hormonal responses to stress in rhesus macaques. Subjects were 10 abusive mothers and their infants, and 10 nonabusive mother-infant pairs. Mothers and infants were genotyped for the rh5-HTTLPR, and studied in the first 6 months of infant life. For mothers and infants, we measured social group behavior, behavioral responses to handling procedures, and plasma concentrations of ACTH and cortisol under basal conditions and in response to stress tests. The proportion of individuals carrying the short rh5-HTTLPR allele was significantly higher among abusive mothers than controls. Among mothers and infants, the short allele was associated with higher basal cortisol levels and greater hormonal stress responses in the infants. In addition, infants who carried the short rh5-HTTLPR allele had higher anxiety scores than infants homozygous for the long allele. The rh5-HTTLPR genotype also interacted with early adverse experience to impact HPA axis function in the infants. These results are consistent with those of previous studies which demonstrate associations between serotonergic activity and anxiety and stress reactivity, and add additional evidence suggesting that genetic variation in serotonergic function may contribute to the occurrence of abusive parenting in rhesus macaques and modulate emotional behavior and HPA axis function.
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“Social buffering of the infant is a dynamic process that wanes as individuals across species mature and become independent (Gee et al., 2014, Levine, 2001, McCormack et al., 2009, Sanchez, 2006, Stanton and Levine, 1990, Suchecki et al., 1995, van Oers et al., 1998) (Fig. 1).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as McCormack et al., 2009
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BackgroundResultInfluentialRole of genotype in the cycle of violence in maltreated children
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., Taylor, A., & Poulton, R. (2002) · Science · doi:10.1126/science.1072290 · Cited by 4,842
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Plotsky, P. M., Owens, M. J., & Nemeroff, C. B. (1998) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(05)70006-x · Cited by 672
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Early experience and serotonin transporter gene variation interact to influence primate CNS function
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Self-citationKendler, K., Kuhn, J. W., Vittum, J., Prescott, C., & Riley, B. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.5.529 · Cited by 647 · cited 1×
“In the current study we found that abused infants with the l/s genotype had higher rates of anxiety and increased HPA axis stress reactivity, which is compelling given the consistency with previous human (Caspi et al., 2003; Kendler et al., 2005) and nonhuman primate literature (Barr et al.”
ResultUher, R., & McGuffin, P. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002067 · Cited by 508 · cited 1×
“We have also chosen this approach, as opposed to evaluating the l/s and s/s animals together in one group, based on recent evidence in the literature suggesting that the short allele may not always be additive in its effects, a phenomenon known as negative heterosis (Middeldorp et al., 2007; Uher and McGuffin, 2008),…”
ResultDiverse patterns of neuroendocrine activity in maltreated children
Cicchetti, D., & Rogosch, F. A. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003145 · Cited by 432 · cited 1×
“, 1998) and in human children and adults with early life stress (Cicchetti and Rogosch, 2001; Gunnar and Vazquez, 2001; Heim et al., 2001; Tarullo and Gunnar, 2006).”
BackgroundBarr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., Schwandt, M., Champoux, M., Lesch, K. P., Goldman, D., et al. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.12.008 · Cited by 385
Self-citationChampoux, M. C., Bennett, A. J., Shannon, C., Higley, J. D., Lesch, K., & Suomi, S. J. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001157 · Cited by 367
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“This association between the short 5-HTTLPR allele and HPA axis reactivity is of importance, as serotonin is directly involved in the activation and negative feedback of the HPA axis (Cassan and D'mello, 2001; Lowry, 2002).”
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Lanfumey, L., Mongeau, R., Cohen‐Salmon, C., & Hamon, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.006 · Cited by 357 · cited 1×
“Altogether, these findings are consistent with the important role of serotonin regulating not only HPA stress reactivity, but its negative feedback (Lanfumey et al., 2008; Porter et al., 2004).”
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The behaviour of socially living rhesus monkeys in their first two and a half years
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Stress Neurobiology and Developmental Psychopathology
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Zeitzer, J. M., Buckmaster, C. L., Parker, K. J., Hauck, C. M., Lyons, D. M., & Mignot, E. J.-M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03555.2003 · Cited by 278 · cited 1×
“Mother–infant pairs were captured and released twice at each age, on different days, to obtain an early morning sample (at sunrise) and an evening sample (at sunset) for analysis of diurnal cortisol secretion (Sanchez et al., 2005; Zeitzer et al., 2003).”
MethodBarr, C. S., Newman, T. K., Becker, M. L., Parker, C. C., Champoux, M. C., Lesch, K., Goldman, D. A., Suomi, S. J., & Higley, J. D. (2003) · Genes Brain & Behavior · doi:10.1046/j.1601-1848.2003.00051.x · Cited by 267
Self-citationSocial Adversity, the Serotonin Transporter (5-HTTLPR) Polymorphism and Major Depressive Disorder
Surtees, P. G., Wainwright, N. W. J., Willis-Owen, S. A. G., Luben, R., Day, N. E., & Flint, J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.014 · Cited by 265 · cited 1×
“Although a recent study failed to replicate these findings (Surtees et al., 2006), other groups have found similar gene by environment effects, such as Kaufman et al.”
ResultLight Affects Morning Salivary Cortisol in Humans
Scheer, F. A. J. L., & Buijs, R. M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.9.6102 · Cited by 258
Newman, T. K., Syagailo, Y. V., Barr, C. S., Wendland, J. R., Champoux, M., Grässle, M., Suomi, S. J., Higley, J. D., & Lesch, K. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.10.012 · Cited by 257
Self-citationRole of the Serotonin Transporter Promoter Polymorphism in Anxiety-Related Traits
Mazzanti, C. M., Lappalainen, J., Long, J. C., Bengel, D., Naukkarinen, H., Eggert, M., Virkkunen, M. E., Linnoila, M., & Goldman, D. A. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.10.936 · Cited by 251 · cited 3×
“Of the two common alleles (long (l) and short (s)), the short (low 5-HTT activity) allele has been associated with higher neuroticism and anxiety (Greenberg et al., 2000; Lesch et al., 1996; Mazzanti et al., 1998; Osher et al., 2000), suicide attempts (Baca-Garcia et al.”
BackgroundResult(1974) · University of Toronto Press eBooks · doi:10.3138/9781487575663 · Cited by 231
Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys
Dario Maestripieri, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504122102 · Cited by 213 · cited 2×
“In that study, approximately half of the female infants that were physically abused by their biological or foster mothers in their first month of life exhibited abusive parenting with their own offspring (Maestripieri, 2005), and the group of abused females that later became abusive mothers had lower CSF levels of 5-H…”
BackgroundResultSelf-citationBarr, C. S., Newman, T. K., Schwandt, M. L., Shannon, C., Dvoskin, R. L., Lindell, S. G., Taubman, J., Thompson, B., Champoux, M., Lesch, K., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403763101 · Cited by 205
Self-citationSánchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., & Winslow, J. T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.032 · Cited by 178 · cited 2×
“This pattern of higher followed by lower basal cortisol levels detected in the abused infants after the first month is consistent with similar effects observed inmonkeys exposed to other early adverse experiences (Capitanio et al., 2005; Clarke et al., 1998; Dettling et al., 2002; Sanchez et al., 2005; Shannon et al.,…”
MethodResultBarr, C. S., Newman, T. K., Becker, M. L., Champoux, M., Lesch, K., Suomi, S. J., Goldman, D. A., & Higley, J. D. (2003) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000067976.62827.ed · Cited by 169
Self-citationCorticosteroid–serotonin interactions in depression: a review of the human evidence
Porter, R. J., Gallagher, P., Watson, S., & Young, A. H. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1774-1 · Cited by 169
Capitanio, J. P., Mendoza, S. P., Mason, W. A., & Maninger, N. (2005) · Developmental Psychobiology · doi:10.1002/dev.20067 · Cited by 153 · cited 1×
“This pattern of higher followed by lower basal cortisol levels detected in the abused infants after the first month is consistent with similar effects observed inmonkeys exposed to other early adverse experiences (Capitanio et al., 2005; Clarke et al., 1998; Dettling et al., 2002; Sanchez et al., 2005; Shannon et al.,…”
ResultThe biology of human parenting: insights from nonhuman primates
Dario Maestripieri, A. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00042-6 · Cited by 152
Self-citationSchneider, M. L., & Suomi, S. J. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80021-l · Cited by 141 · cited 1×
“The scales used to assess the infants reactivity were adapted from two sources: 1) the Behavioral Temperament Scale (Ruppenthal and Sackett, 1992), and 2) the state control portion of the Neonatal Neurobehavioral Assessment (Schneider and Suomi, 1992) that provides measures of temperament, in addition to orientation a…”
MethodMaestripieri, D., Higley, J. D., Lindell, S. G., Newman, T. K., McCormack, K. M., & Sánchez, M. M. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.5.1017 · Cited by 129 · cited 5×
“, 2006; Troisi and D'Amato, 1991), and, interestingly, a recent study suggests that altered serotonergic function may be one of the mechanisms underlying the intergenerational transmission of infant abuse in rhesus monkeys (Maestripieri et al., 2006).”
BackgroundResultInfluentialSelf-citationOsher, Y., Hamer, D. H., & Benjamin, J. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000660 · Cited by 127 · cited 3×
“Of the two common alleles (long (l) and short (s)), the short (low 5-HTT activity) allele has been associated with higher neuroticism and anxiety (Greenberg et al., 2000; Lesch et al., 1996; Mazzanti et al., 1998; Osher et al., 2000), suicide attempts (Baca-Garcia et al.”
BackgroundResultDefensive Behaviors in Infant Rhesus Monkeys: Ontogeny and Context-Dependent Selective Expression
Kalin, N. H., Shelton, S. E., & Takahashi, L. K. (1991) · Child Development · doi:10.1111/j.1467-8624.1991.tb01598.x · Cited by 120 · cited 1×
“This may be due to the fact that this is a critical developmental period for rhesus macaques, with fearful behavior becoming more prevalent and regulated (Kalin et al., 1991), in parallel to an increase in exploratory behavior and an increase in responsibility of keeping in contact with the mother (Hinde and SpencerBo…”
BackgroundParenting styles of abusive mothers in group-living rhesus macaques
Maestripieri, D. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0578 · Cited by 116 · cited 5×
“Abuse events did not last more than a few seconds and therefore only frequencies were recorded, as is the standard for this type of research (Maestripieri, 1998; Troisi and D'Amato, 1983).”
BackgroundMethodInfluentialSelf-citationIntergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms
Dario Maestripieri, A., Lindell, S. G., & Higley, J. D. (2007) · Developmental Psychobiology · doi:10.1002/dev.20200 · Cited by 110 · cited 1×
“, 2006) and with evidence that high rates of infant rejection is also associated with low CSF 5-HIAA levels in the mothers (Maestripieri et al., 2007).”
BackgroundSelf-citationMcCormack, K., Sanchez, M. M., Bardi, M., & Maestripieri, D. (2006) · Developmental Psychobiology · doi:10.1002/dev.20157 · Cited by 102 · cited 7×
“Previous studies in nonhuman primates have also characterized abusive mothers as having higher levels of anxiety and being more rejecting of their infants (McCormack et al., 2006; Maestripieri, 1998; Troisi and D'Amato, 1984).”
BackgroundMethodInfluentialSelf-citationLichtermann, D., Hranilović, D., Trixler, M., Franke, P. E., Jernej, B., Delmo, C. D., Knapp, M., Schwab, S. G., Maier, W., & Wildenauer, D. B. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.12.2045 · Cited by 99
Bethea, C. L., Streicher, J. M., Coleman, K., Pau, F. K.-Y., Moessner, R., & Cameron, J. L. (2004) · Behavior Genetics · doi:10.1023/b:bege.0000017873.61607.be · Cited by 96 · cited 2×
“As in humans, rhesus monkeys with one or more copies of the short allele exhibit greater levels of anxiety and are more behaviorally reactive on temperament tests than individuals homozygous for the long allele (Bethea et al., 2004; Champouxet al., 2002).”
BackgroundResultDettling, A. C., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00785-2 · Cited by 95 · cited 1×
“This pattern of higher followed by lower basal cortisol levels detected in the abused infants after the first month is consistent with similar effects observed inmonkeys exposed to other early adverse experiences (Capitanio et al., 2005; Clarke et al., 1998; Dettling et al., 2002; Sanchez et al., 2005; Shannon et al.,…”
ResultMiddeldorp, C. M., de Geus, E. J. C., Beem, A. L., Lakenberg, N., Hottenga, J., Slagboom, P. E., & Boomsma, D. I. (2007) · Behavior Genetics · doi:10.1007/s10519-006-9139-7 · Cited by 89 · cited 1×
“We have also chosen this approach, as opposed to evaluating the l/s and s/s animals together in one group, based on recent evidence in the literature suggesting that the short allele may not always be additive in its effects, a phenomenon known as negative heterosis (Middeldorp et al., 2007; Uher and McGuffin, 2008),…”
ResultDefensive Behaviors in Infant Rhesus Monkeys: Ontogeny and Context-Dependent Selective Expression
Kalin, N. H., Shelton, S. E., & Takahashi, L. K. (1991) · Child Development · doi:10.2307/1131161 · Cited by 88
Hinde, R. A., & McGinnis, L. M. (1977) · Psychological Medicine · doi:10.1017/s0033291700029275 · Cited by 84 · cited 1×
“Mother–infant separations at this age cause known behavioral and HPA axis stress responses in rhesus monkey mothers and infants (Bowlby, 1968; Hinde and McGinnis, 1977; for review see Sanchez et al., 2001).”
Background5-HT-HPA Interactions in Two Models of Transgenic Mice Relevant to Major Depression
Lanfumey, L., la Cour, C. M., Froger, N., & Hamon, M. (2000) · Neurochemical Research · doi:10.1023/a:1007683810230 · Cited by 78 · cited 1×
“In addition, targeted disruption of the serotonin transporter gene in rodents also results in increased HPA axis responses to stress (Lanfumey et al., 2000).”
BackgroundA Gender-Specific Association between the Serotonin Transporter Gene and Suicide Attempts
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Risk Factors for Infant Abuse and Neglect in Group-Living Rhesus Monkeys
Maestripieri, D., & Carroll, K. A. (1998) · Psychological Science · doi:10.1111/1467-9280.00027 · Cited by 76 · cited 1×
“Previous research indicates that infant abuse is concentrated along specific matrilines in both rhesus and pigtail macaques, such that daughters of abusive mothers are more likely to abuse their own offspring than those of non-abusivemothers (Maestripieri and Carroll, 1998;Maestripieri et al., 1997b).”
BackgroundSelf-citationInfant abuse runs in families of group-living pigtail macaques
Maestripieri, D., Wallen, K., & Carroll, K. A. (1997) · Child Abuse & Neglect · doi:10.1016/s0145-2134(97)00006-9 · Cited by 75
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Ontogeny of Luteinizing Hormone Secretion and First Ovulation in Seasonal Breeding Rhesus Monkeys*
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“, 1983) and that infants who have experienced these procedures exhibit no alterations in normal development (Wilson et al., 1986).”
BackgroundMos, J., Lammers, J. H. C. M., van der Poel, A. M., Bermond, B., Meelis, W., & Kruk, M. R. (1983) · Aggressive Behavior · doi:10.1002/1098-2337(1983)9:2 · Cited by 57
Sánchez, M. M., Alagbe, O., Felger, J. C., Zhang, J., Graff, A., Grand, A. P., Maestripieri, D., & Miller, A. H. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002025 · Cited by 54 · cited 1×
“We have previously characterized the behavioral, neuroendocrine and neurochemical correlates of abusive mothering, and the developmental consequences of infant abuse in the offspring (Maestripieri et al., 2006; McCormack et al., 2006; McCormack et al., submitted for publication; Sanchez et al., 2007).”
BackgroundLight Affects Morning Salivary Cortisol in Humans
Scheer, F. A. J. L. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.9.3395 · Cited by 53
Ambivalence in Monkey Mothering
Troisi, A., & D'Amato, F. R. (1984) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-198402000-00007 · Cited by 46 · cited 1×
“Previous studies in nonhuman primates have also characterized abusive mothers as having higher levels of anxiety and being more rejecting of their infants (McCormack et al., 2006; Maestripieri, 1998; Troisi and D'Amato, 1984).”
BackgroundClarke, A. S., Kraemer, G. W., & Kupfer, D. J. (1998) · Psychiatry Research · doi:10.1016/s0165-1781(98)00032-8 · Cited by 43 · cited 1×
“This pattern of higher followed by lower basal cortisol levels detected in the abused infants after the first month is consistent with similar effects observed inmonkeys exposed to other early adverse experiences (Capitanio et al., 2005; Clarke et al., 1998; Dettling et al., 2002; Sanchez et al., 2005; Shannon et al.,…”
ResultCassano, W. J., & D’mello, A. P. (2001) · Neuroendocrinology · doi:10.1159/000054683 · Cited by 41
Joiner, T. E., Johnson, F., Soderstrom, K., & Brown, J. S. (2003) · Journal of Affective Disorders · doi:10.1016/s0165-0327(02)00171-4 · Cited by 31
Anxiety in the pathogenesis of primate infant abuse: a pharmacological study
Troisi, A., & D'Amato, F. R. (1991) · Psychopharmacology · doi:10.1007/bf02244261 · Cited by 30
Maestripieri, D. (1994) · American Journal of Primatology · doi:10.1002/ajp.1350320105 · Cited by 30 · cited 1×
“Previous research found an association between abusive behavior and increased anxiety in these mothers (Maestripieri, 1994; McCormack et al., 2006; Troisi and D'Amato, 1991), and, interestingly, a recent study suggests that altered serotonergic function may be one of the mechanisms underlying the intergenerational tra…”
BackgroundSelf-citation1. Mother/Infant Relations in Rhesus Monkeys
Hinde, R. A. (1974) · University of Toronto Press eBooks · doi:10.3138/9781487575663-004 · Cited by 26
Effects on behaviour of disruption of an affectional bond.
Bowlby, J. (1968) · PubMed · Cited by 23
Passamani, M. (1998) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1998)46:4
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“, 1997), and enhanced stress response (McCormack et al., 2009), future studies need to examine the impact of maternal HFD consumption on neuronal development, stress response, and cognition.”
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Metadata
- Authors
- McCormack, K., Newman, T. K., Higley, J. D., Maestripieri, D., & Sanchez, M. M.
- Affiliations
- Spelman College (US)
- University of Cape Town (ZA)
- Brigham Young University (US)
- Corresponding author
- McCormack, K.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2009-04
- Volume
- 55
- Issue
- 4
- Pages
- 538-547
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC3954512
- OpenAlex
- W2068680756
- Cited by
- 161
- References
- 73
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 7 · 2021: 2 · 2020: 21 · 2019: 8 · 2018: 10 · 2017: 5 · 2016: 11 · 2015: 7 · 2014: 9 · 2013: 11 · 2012: 17
- FWCI
- 6.36
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH62577, MH65046, P50MH058922, MH58922, MH63097, K02MH063097, R01MH062577, MH065046, R21MH065046)
- National Institute of General Medical Sciences (K12-GM 00680, K12GM000680)
- National Center for Research Resources (RR-00 165, P51RR000165)
- National Institute on Minority Health and Health Disparities (P20MD000215, MD000215)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Keywords
- serotonin transporter gene, 5-HTTLPR, infant abuse, abusive parenting, rhesus monkeys, hypothalamic-pituitary-adrenal axis, cortisol, ACTH, stress reactivity, anxiety, early life stress, gene-environment interaction
- MeSH terms
- Adrenocorticotropic Hormone, Aging, Animals, Anxiety, Female, Hormones, Hydrocortisone, Hypothalamo-Hypophyseal System, Macaca mulatta, Maternal Behavior, Maternal Deprivation, Mothers, Pituitary-Adrenal System, Social Behavior, Stress, Psychological, Time Factors, Genetic Variation, Sequence Analysis, DNA, Serotonin Plasma Membrane Transport Proteins
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