Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

McCormack, K.; Newman, T.K.; Higley, J.D.; Maestripieri, D.; Sanchez, M.M.

doi:10.1016/j.yhbeh.2009.01.009

Cited by 161Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behavior

Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

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McCormack, K., Newman, T.K., Higley, J.D., Maestripieri, D., Sanchez, M.M.·2009·Hormones and Behavior

DOI 10.1016/j.yhbeh.2009.01.009PMC PMC3954512

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Abstract

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.
“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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Result
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BackgroundResultInfluential
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Background
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Background
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Method
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Background
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Result
A novel functional polymorphism within the promoter of the serotonin transporter gene: possible role in susceptibility to affective disorders.
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Self-citation
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Result
Diverse patterns of neuroendocrine activity in maltreated children
Cicchetti, D., & Rogosch, F. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003145 · Cited by 437 · cited 1× · see citing works
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Background
Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques
Barr, 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 · see citing works
Self-citation
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Background
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Method
The utility of the non‐human primate model for studying gene by environment interactions in behavioral research
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Self-citation
Social Adversity, the Serotonin Transporter (5-HTTLPR) Polymorphism and Major Depressive Disorder
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Light Affects Morning Salivary Cortisol in Humans
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Self-citation
Role of the Serotonin Transporter Promoter Polymorphism in Anxiety-Related Traits
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“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
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BackgroundResultSelf-citation
Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques
Barr, 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 · see citing works
Self-citation
Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing
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“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.,…”
MethodResult
Serotonin Transporter Gene Variation is Associated with Alcohol Sensitivity in Rhesus Macaques Exposed to Early‐Life Stress
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Self-citation
Corticosteroid–serotonin interactions in depression: a review of the human evidence
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“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.,…”
Result
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Self-citation
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Method
Association and linkage of anxiety-related traits with a functional polymorphism of the serotonin transporter gene regulatory region in Israeli sibling pairs
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“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
Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta).
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BackgroundResultInfluentialSelf-citation
Parenting 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× · see citing works
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BackgroundMethodInfluentialSelf-citation
Early deprivation and behavioral and physiological responses to social separation/novelty in the marmoset
Dettling, A. C., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00785-2 · Cited by 113 · cited 1× · see citing works
“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.,…”
Result
Intergenerational 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× · see citing works
“, 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-citation
Defensive Behaviors in Infant Rhesus Monkeys: Ontogeny and Context-dependent Selective Expression
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Background
Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life
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BackgroundMethodInfluentialSelf-citation
Support for Allelic Association of a Polymorphic Site in the Promoter Region of the Serotonin Transporter Gene With Risk for Alcohol Dependence
Lichtermann, 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 · see citing works
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“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).”
BackgroundResult
Family Based Association Analyses between the Serotonin Transporter Gene Polymorphism (5-HTTLPR) and Neuroticism, Anxiety and Depression
Middeldorp, 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 91 · cited 1× · see citing works
“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),…”
Result
Schizophrenia and smoking: Evidence for a common neurobiological basis?
Stassen, H. H., Bridler, R., H�gele, S., Hergersberg, M., Mehmann, B., Schinzel, A., Weisbrod, M., & Scharfetter, C. (2000) · American Journal of Medical Genetics · doi:10.1002/(sici)1096-8628(20000403)96:2 · Cited by 89 · see citing works
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“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).”
Background
5-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× · see citing works
“In addition, targeted disruption of the serotonin transporter gene in rodents also results in increased HPA axis responses to stress (Lanfumey et al., 2000).”
Background
A Gender-Specific Association between the Serotonin Transporter Gene and Suicide Attempts
Baca‐García, E. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00394-3 · Cited by 78 · see citing works
Risk Factors for Infant Abuse and Neglect in Group-Living Rhesus Monkeys
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“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-citation
Infant 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 · see citing works
Self-citation
Effects of capture and venipuncture on serum levels of prolactin, growth hormone and cortisol in outdoor compound-housed female rhesus monkeys (Macaca mulatta)
Blank, M. S., Gordon, T. P., & Wilson, M. E. (1983) · European Journal of Endocrinology · doi:10.1530/acta.0.1020190 · Cited by 72 · see citing works
Ontogeny of Luteinizing Hormone Secretion and First Ovulation in Seasonal Breeding Rhesus Monkeys*
Wilson, M. E., GORDON, T. P., & Collins, D. C. (1986) · Endocrinology · doi:10.1210/endo-118-1-293 · Cited by 70 · cited 1× · see citing works
“, 1983) and that infants who have experienced these procedures exhibit no alterations in normal development (Wilson et al., 1986).”
Background
Effects of midbrain central gray lesions on spontaneous and electrically induced aggression in the rat
Mos, 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 · see citing works
Activated p38 MAPK is associated with decreased CSF 5-HIAA and increased maternal rejection during infancy in rhesus monkeys
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× · see citing works
“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).”
Background
Light 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 · see citing works
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× · see citing works
“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).”
Background
Effects of rearing condition on HPA axis response to fluoxetine and desipramine treatment over repeated social separations in young rhesus monkeys
Clarke, A. S., Kraemer, G. W., & Kupfer, D. J. (1998) · Psychiatry Research · doi:10.1016/s0165-1781(98)00032-8 · Cited by 43 · cited 1× · see citing works
“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.,…”
Result
Acute Stress-Induced Facilitation of the Hypothalamic-Pituitary-Adrenal Axis: Evidence for the Roles of Stressor Duration and Serotonin
Cassano, W. J., & D’mello, A. P. (2001) · Neuroendocrinology · doi:10.1159/000054683 · Cited by 41 · see citing works
Is there an association between serotonin transporter gene polymorphism and family history of depression?
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 · see citing works
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 · see citing works
Infant abuse associated with psychosocial stress in a group‐living pigtail macaque (Macaca nemestrina) Mother
Maestripieri, D. (1994) · American Journal of Primatology · doi:10.1002/ajp.1350320105 · Cited by 30 · cited 1× · see citing works
“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-citation
1. Mother/Infant Relations in Rhesus Monkeys
Hinde, R. A. (1974) · University of Toronto Press eBooks · doi:10.3138/9781487575663-004 · Cited by 26 · see citing works
Effects on behaviour of disruption of an affectional bond.
Bowlby, J. (1968) · PubMed · Cited by 23 · see citing works
Untitled work
Passamani, M. (1998) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1998)46:4
Untitled work
(1997) · doi:10.1002/(sici)1098-2302(199711)31:3

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Adolescent risk taking, impulsivity, and brain development: Implications for prevention
Romer, D. (2010) · Developmental Psychobiology · doi:10.1002/dev.20442 · Cited by 691 · see citing works
Chronic Consumption of a High-Fat Diet during Pregnancy Causes Perturbations in the Serotonergic System and Increased Anxiety-Like Behavior in Nonhuman Primate Offspring
Sullivan, E. L., Grayson, B. E., Takahashi, D. L., Robertson, N. D., Maier, A., Bethea, C. L., Smith, M. S., Coleman, K., & Grove, K. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5560-09.2010 · Cited by 324 · see citing works
“, 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.”
Background
Elucidating the etiology of individual differences in parenting: A meta-analysis of behavioral genetic research.
Klahr, A. M., & Burt, S. A. (2013) · Psychological Bulletin · doi:10.1037/a0034205 · Cited by 258 · see citing works
Empathy from infancy to adolescence: An attachment perspective on the development of individual differences
Stern, J. A., & Cassidy, J. (2018) · Developmental Review · doi:10.1016/j.dr.2017.09.002 · Cited by 222 · see citing works
Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates
Parker, K. J., & Dario Maestripieri, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.003 · Cited by 192 · see citing works
The serotonin transporter gene-linked polymorphic region (5-HTTLPR) and cortisol stress reactivity: a meta-analysis
Miller, R. E., Wankerl, M., Tobias Stalder, A., Kirschbaum, C., & Alexander, N. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.124 · Cited by 177 · see citing works
Early life adversity shapes neural circuit function during sensitive postnatal developmental periods
Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177 · see citing works
“Similarly, rhesus macaques with the S allele who experience ELA show heightened stress responses, reduced serotonergic function, and greater anxiety than L allele carriers [170], and mice with disrupted 5-HTT show enhanced ACTH levels in response to stress [171].”
Background
Variations in the serotonin-transporter gene are associated with attention bias patterns to positive and negative emotion faces
Pérez‐Edgar, K. E., Bar‐Haim, Y., McDermott, J. M., Gorodetsky, E. K., Hodgkinson, C. A., Goldman, D. A., Monique Ernst, D., Pine, D. S., & Fox, N. A. (2009) · Biological Psychology · doi:10.1016/j.biopsycho.2009.08.009 · Cited by 171 · see citing works
“The data suggest that this reduction amplifies the individual’s response to threat, evident in hyper-reactive neuroendocrine (Jabbi et al., 2007; McCormack et al., 2009) and amygdala (Hariri et al.”
Background
Parental buffering of fear and stress neurobiology: reviewing parallels across rodent, monkey, and human models
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1070198 · Cited by 158 · see citing works
The neuroendocrinology of primate maternal behavior
Wendy Saltzman, A., & Dario Maestripieri, A. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.09.017 · Cited by 150 · see citing works
“(McCormack et al., 2009) suggests that genetically based variation in brain serotonergic function may also play a role in the manifestation of abusive parenting and its transmission across generations.”
Background
Maternal early life experiences and parenting: the mediating role of cortisol and executive function
Gonzalez, A., Jenkins, J. M., Steiner, M., & Fleming, A. S. (2012) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2012.04.003 · Cited by 146 · see citing works
Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits
Sánchez, M. M., McCormack, K. M., & Howell, B. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087426 · Cited by 135 · see citing works
“Although there is no solid evidence of a true SHRP in rhesus monkeys, socially familiar cues, specifically the presence of a nurturing mother, do buffer the HPA axis stress responses in infant rhesus macaques (McCormack et al., 2009; Sanchez, 2006).”
Self-citation
Serotonin transporter expression is predicted by early life stress and is associated with disinhibited behavior in infant rhesus macaques
Kinnally, E. L., Tarara, E. R., Mason, W. A., Mendoza, S. P., Abel, K., Lyons, L. A., & Capitanio, J. P. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00533.x · Cited by 125 · see citing works
“This is consistent with our previous work [Kinnally et al. 2008; Kinnally et al.(in press)], but inconsistent with other work in rhesus macaques (Barr et al. 2004; Bennett et al. 2002; Champoux et al. 2002; McCormack et al. 2009; Spinelli et al. 2007).”
Influential
Brain white matter microstructure alterations in adolescent rhesus monkeys exposed to early life stress: associations with high cortisol during infancy
Howell, B., McCormack, K. M., Grand, A. P., Sawyer, N. T., Zhang, X., Maestripieri, D., Hu, X. P., & Sánchez, M. M. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-21 · Cited by 107 · see citing works
“Using this model we have previously reported increased emotional reactivity in maltreated infants and juveniles [7,9,70] and social alterations including delayed independence from the mother and less play during infancy [6,71], as well as increased social aggression during adolescence [72].”
InfluentialSelf-citation
Genetics of anxiety disorders: the complex road from DSM to DNA
Smoller, J. W., Block, S. R., & Young, M. M. (2009) · Depression and Anxiety · doi:10.1002/da.20623 · Cited by 99 · see citing works
Models of stress in nonhuman primates and their relevance for human psychopathology and endocrine dysfunction
Meyer, J. S., & Hamel, A. F. (2014) · ILAR Journal · doi:10.1093/ilar/ilu023 · Cited by 96 · see citing works
Genetics of Resilience: Gene-by-Environment Interaction Studies as a Tool to Dissect Mechanisms of Resilience.
Elbau, I., Cruceanu, C., & Binder, E. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.025 · Cited by 91 · see citing works
Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior
Opendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
“Social buffering of the infant is a dynamic process that wanes s individuals across species mature and become independent Gee et al., 2014; Levine, 2001; McCormack et al., 2009; Sanchez, 006; Stanton and Levine, 1990; Suchecki et al., 1995; van Oers t al., 1998) (Fig.”
Steroid hormones, stress and the adolescent brain: A comparative perspective
Brown, G. R., & Spencer, K. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.016 · Cited by 86 · see citing works
“In 23 primates, basal CORT levels rise during adolescence (e.g., chimpanzees, Pan troglodytes: 24 Seraphin et al., 2008; rhesus macaques, McCormack et al., 2009) , and studies of human 25 adolescents have reported enhanced stress reactivity in adolescents compared to children (e.g., 1 Gunnar et…”
Childhood adversity and allostatic overload of the hypothalamic–pituitary–adrenal axis: A vulnerability model for depressive disorders
Wilkinson, P. O., & Goodyer, I. M. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000472 · Cited by 86 · see citing works
“Genotype may moderate HPAA response to stress (McCormack et al., 2009).”
BackgroundResultInfluential
Epigenetic dynamics in psychiatric disorders: Environmental programming of neurodevelopmental processes
Kofink, D., Boks, M. P. M., Timmers, H. T. M., & Kas, M. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.020 · Cited by 83 · see citing works
Maternal influences on primate social development
Dario Maestripieri, A. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2547-x · Cited by 77 · see citing works
Early adverse experience increases emotional reactivity in juvenile rhesus macaques: Relation to amygdala volume
Howell, B. R., Grand, A. P., McCormack, K. M., Shi, Y., LaPrarie, J. L., Maestripieri, D., Styner, M. A., & Sanchez, M. M. (2014) · Developmental Psychobiology · doi:10.1002/dev.21237 · Cited by 72 · see citing works
“…and inclusion/exclusion criteria described in detail for this species in previous publications (e.g. Maestripieri, 1998; McCormack et al., 2006; McCormack et al., 2009; Troisi & D’Amato, 1983), infants were classified as abused if the mother was observed exhibiting at least 3 instances of the…”
Self-citation
The Parental Brain
Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques Macaca mulatta
Higham, J. P., Barr, C. S., Hoffman, C. L., Mandalaywala, T. M., Parker, K. J., & Maestripieri, D. (2011) · Behavioral Neuroscience · doi:10.1037/a0022695 · Cited by 69 · see citing works
“Genetic polymorphisms (e.g., in or related to dopamine receptor genes and the serotonin transporter gene; Fairbanks et al., 2006; McCormack et al., 2009) and neuroendocrine variables (e.g., reproductive and stress hormones, endogenous opioids and oxytocin (OT), and monoamine neurotransmitters;…”
The role of childhood abuse in HPA-axis reactivity in Social Anxiety Disorder: A pilot study
Elzinga, B. M., Spinhoven, P., Berretty, E. W., de Jong, P., & Karin Roelofs, A. (2009) · Biological Psychology · doi:10.1016/j.biopsycho.2009.09.006 · Cited by 67 · see citing works
“Interestingly, some of these same genes also appear to be associated with alterations in HPA-axis reactivity after stress exposure (Binder et al., 2008; McCormack et al., 2009; see also Ouellet-Morin et al., 2008).”
Background
Becoming DADS
Gettler, L. T. (2016) · Current Anthropology · doi:10.1086/686149 · Cited by 66 · see citing works
“Finally, these researchers (Champoux et al. 2002; Jedema et al. 2009) and others (McCormack et al. 2009) have found a number of significant serotonin transporter gene X rearing environment interactions that predict monkeys’ behaviors from infancy through adulthood.”
Background
Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering
Aïn, S. A., Perry, R. E., Nuñez, B. S., Kayser, K. E., Hochman, C., Brehman, E., LaComb, M., Wilson, D. A., & Sullivan, R. M. (2016) · Social Neuroscience · doi:10.1080/17470919.2016.1159605 · Cited by 63 · see citing works
Interaction of the Serotonin Transporter-Linked Polymorphic Region and Environmental Adversity: Increased Amygdala-Hypothalamus Connectivity as a Potential Mechanism Linking Neural and Endocrine Hyperreactivity
Alexander, N., Klucken, T., Koppe, G., Osinsky, R., Walter, B., Vaitl, D., Sammer, G., Stark, R. M., & Hennig, J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.030 · Cited by 62 · see citing works
Cross-fostering: Elucidating the effects of gene×environment interactions on phenotypic development
McCarty, R. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.025 · Cited by 61 · see citing works
Understanding behavioral effects of early life stress using the reactive scope and allostatic load models
Howell, B., & Sánchez, M. M. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000460 · Cited by 58 · see citing works
Gestational stress and fluoxetine treatment differentially affect plasticity, methylation and serotonin levels in the PFC and hippocampus of rat dams
Gemmel, M., Rayen, I., van Donkelaar, E. L., Loftus, T., Steinbusch, H. W. M., Kokras, N., Dalla, C., & Pawluski, J. L. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.068 · Cited by 56 · see citing works
“Rhesus macaque mothers who demonstrate abusive mothering traits also show short allele variants of the serotonin transporter gene which is further associated with increased basal cortisol levels (McCormack et al., 2009).”
The serotonin transporter gene and functional and pathological adaptation to environmental variation across the life span
Homberg, J. R., & van den Hove, D. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.08.003 · Cited by 51 · see citing works
“abuse, to impact upon HPA axis function in the infants (McCormack et al., 2009).”
The impact of adverse life events and the serotonin transporter gene promoter polymorphism on the development of eating disorder symptoms
Akkermann, K., Kaasik, K., Kiive, E., Nordquist, N., Oreland, L., & Harro, J. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.09.013 · Cited by 52 · see citing works
Affective and neuroendocrine stress reactivity to an academic examination: Influence of the 5-HTTLPR genotype and trait neuroticism
Verschoor, E., & Markus, C. R. (2011) · Biological Psychology · doi:10.1016/j.biopsycho.2011.06.001 · Cited by 48 · see citing works
Maternal buffering beyond glucocorticoids: impact of early life stress on corticolimbic circuits that control infant responses to novelty
Howell, B., McMurray, M. S., Guzman, D., Nair, G., Shi, Y., McCormack, K. M., Hu, X. P., Styner, M. A., & Sánchez, M. M. (2016) · Social Neuroscience · doi:10.1080/17470919.2016.1200481 · Cited by 46 · see citing works
“Behavioral observations were collected in each mother-infant pair by four experienced coders from observation towers located at each social compound during the first three months postpartum using an adaptation of a well-established rhesus monkey ethogram (Altmann, 1962) and following previously published procedures (M…”
BackgroundMethodInfluentialSelf-citation
The neurobiology of safety and threat learning in infancy
Dębiec, J., & Sullivan, R. M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.015 · Cited by 45 · see citing works
Nonhuman Primate Models of Depression: Effects of Early Experience and Stress
Worlein, J. M. (2014) · ILAR Journal · doi:10.1093/ilar/ilu030 · Cited by 42 · see citing works
Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi)
Birnie, A. K., Taylor, J. H., Cavanaugh, J., & French, J. A. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.08.011 · Cited by 43 · see citing works
“, 2004) or monoaminergic (Barr et al., 2004b; McCormack et al., 2009) neurotransmitter system components.”
Background
Early Experience Affects the Strength of Vigilance for Threat in Rhesus Monkey Infants
Mandalaywala, T. M., Parker, K. J., & Dario Maestripieri, A. (2014) · Psychological Science · doi:10.1177/0956797614544175 · Cited by 42 · see citing works
“Infants who possess this same variant often demonstrate impaired emotion regulation and heightened anxiety, but only when exposed to early life adversity (e.g., McCormack et al., 2009; Spinelli et al., 2012).”
A comparative approach to affect and cooperation
Massen, J. J. M., Behrens, F., Martin, J. S., Stocker, M., & Brosnan, S. F. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.027 · Cited by 44 · see citing works
Serotonin pathway gene–gene and gene–environment interactions influence behavioral stress response in infant rhesus macaques
Kinnally, E. L., Karere, G. M., Lyons, L. A., Mendoza, S. P., Mason, W. A., & Capitanio, J. P. (2010) · Development and Psychopathology · doi:10.1017/s0954579409990241 · Cited by 41 · see citing works
Sociodemographic risk, parenting, and effortful control: Relations to salivary alpha‐amylase and cortisol in early childhood
Taylor, Z., Spinrad, T. L., VanSchyndel, S. K., Eisenberg, N., Huynh, J., Sulik, M. J., & Granger, D. A. (2012) · Developmental Psychobiology · doi:10.1002/dev.21079 · Cited by 39 · see citing works
Social Subordination Stress and Serotonin Transporter Polymorphisms: Associations With Brain White Matter Tract Integrity and Behavior in Juvenile Female Macaques
Howell, B., Godfrey, J., Gutman, D. A., Michopoulos, V., Zhang, X., Nair, G., Hu, X. P., Wilson, M. E., & Sánchez, M. M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht187 · Cited by 39 · see citing works
“…stress responses and modulate vulnerability to the deleterious effects of early life stress, both in humans (Caspi et al. 2003; Zalsman et al. 2006; Stein et al. 2008; Caspi et al. 2010) and nonhuman primates (Bennett et al. 2002; Champoux et al. 2002; Barr et al. 2004; McCormack et al. 2009).”
Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates
Morin, E. L., Howell, B. R., Feczko, E., Earl, E., Pincus, M., Reding, K., Kovacs-Balint, Z. A., Meyer, J. S., Styner, M., Fair, D., et al. (2020) · Development and Psychopathology · doi:10.1017/s0954579420001133 · Cited by 37 · see citing works
“…impact on development of amygdala FC, which may underlie the increased emotional reactivity reported in maltreated animals (Howell et al., 2014; McCormack et al., 2009; McCormack et al., 2006; Morin et al., 2019; Morin et al., 2018); and (b) whether the prolonged exposure to high cortisol…”
BackgroundMethodInfluential
The development of the hypothalamic–pituitary–adrenal axis in rhesus monkeys: Effects of age, sex, and early experience
Koch, H. R., McCormack, K. M., Sánchez, M. M., & Dario Maestripieri, A. (2012) · Developmental Psychobiology · doi:10.1002/dev.21093 · Cited by 37 · see citing works
“…function under both basal conditions and in response to stress, that the altered response to stress was different in male and female infants, and that this was primarily a short-term effect that was detectable in the first year or life but not in subsequent years (see also McCormack et al., 2009).”
BackgroundSelf-citation
Living in a dangerous world decreases maternal care: A study in serotonin transporter knockout mice
Heiming, R. S., Bodden, C., Jansen, F., Lewejohann, L., Kaiser, S., Lesch, K., Palme, R., & Sachser, N. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.006 · Cited by 36 · see citing works
“Indeed, variation in the frequency and intensity of maternal care, in particular maternal licking and grooming (LG) of pups, is amajor source of interindividual differences in behavioral profile and stress responsiveness in adulthood (Kaufman et al., 2004; McCormack et al., 2009; Meaney, 2001).”
The social evolution of individual differences: Future directions for a comparative science of personality in social behavior
Martin, J. S., Jaeggi, A. V., & Koski, S. E. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104980 · Cited by 35 · see citing works
“, 2016) and rhesus macaques (Macaca mulatta; McCormack et al., 2009) to southern field crickets (Gryllus bimaculatus; Abbey-Lee et al.”
Background
Interaction of serotonin transporter linked polymorphic region and childhood neglect on criminal behavior and substance use for males and females
Vaske, J. C., Newsome, J., & WRIGHT, J. P. (2012) · Development and Psychopathology · doi:10.1017/s0954579411000769 · Cited by 35 · see citing works
“…allele exhibit lower levels of 5-hydroxyindoleacetic acid, exhibit higher levels of ACTH responses to stress, and exhibit more aggressive and anxious behaviors in response to stress than maltreated subjects who do not carry a copy of the short allele (Maestripieri, 2005; McCormack et al., 2009).”
Background
Hormonal effects of maltreatment in Nazca booby nestlings: Implications for the “cycle of violence”
Grace, J. K., Dean, K. M., Ottinger, M. A., & Anderson, D. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.03.007 · Cited by 33 · see citing works
“, 2003); (2) young acquire maltreatment behavior through observational learning (Chapman and Scott, 2001); and (3) maltreatment is a genetically heritable trait (Caspi et al., 2002; Kaufman et al., 2004; McCormack et al., 2009; Widom and Brzustowicz, 2006).”
Shaping long-term primate development: Telomere length trajectory as an indicator of early maternal maltreatment and predictor of future physiologic regulation
Drury, S. S., Howell, B., Jones, C., Esteves, K. C., Morin, E. L., Schlesinger, R. P., Meyer, J. S., Baker, K. C., & Sánchez, M. M. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001225 · Cited by 33 · see citing works
“0.8) from observation towers using established ethograms and procedures (Altmann, 1962; Howell et al., 2017, in press; Maestripieri & Carroll, 1998; McCormack et al., 2009, 2015; McCormack, Sanchez, Bardi, & Maestripieri, 2006).”
MethodInfluential
Glucocorticoids as Predictors of Treatment Response in Depression
Horstmann, S., & Binder, E. B. (2011) · Harvard Review of Psychiatry · doi:10.3109/10673229.2011.586550 · Cited by 30 · see citing works
Early-life social adversity and developmental processes in nonhuman primates
French, J. A., & Carp, S. B. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.004 · Cited by 31 · see citing works
“Increased rates of distress calls are also observed in infant macaques that experienced abuse compared to infants who were not abused [9].”
The development of an instrument to measure global dimensions of maternal care in rhesus macaques (Macaca mulatta)
McCormack, K. M., Howell, B., Guzman, D., Villongco, C., Pears, K. C., Kim, H. K., Gunnar, M. R., & Sánchez, M. M. (2014) · American Journal of Primatology · doi:10.1002/ajp.22307 · Cited by 32 · see citing works
“…by four experienced coders from observation towers situated over each social compound, during thefirst 3months postpartumusing an adaptation of a well‐established rhesus monkey ethogram [Altmann, 1962], following previously published procedures [Maestripieri, 1998; McCormack et al., 2006, 2009].”
Self-citation
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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.
ORCID: McCormack, K.
Higley, J.D.
Venue: Hormones and Behavior
Publisher: Elsevier BV
Published: 2009-04
Volume: 55
Issue: 4
Pages: 538-547
ISSN: 0018-506X (ISSN-L)
DOI: 10.1016/j.yhbeh.2009.01.009
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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
Social Sciences › Psychology › Social Psychology › 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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Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

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