The DOI matches its Crossref record; 71 of the 73 references it cites were found in a registry or an index.
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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Citations
Cites
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · 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.”
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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.”
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
Serotonin transporter genetic variation and the response of the human amygdala.
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The link between childhood trauma and depression: insights from HPA axis studies in humans
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“A wide variety of studies have shown that humans with major depressive disorder exhibit altered HPA axis functioning (Heim et al., 2008; Plotsky et al., 1998).”
BackgroundSÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003
GUNNAR, M. R., & VAZQUEZ, D. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003066 · Cited by 900 · 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).”
BackgroundSocial supports and serotonin transporter gene moderate depression in maltreated children
Kaufman, J., Yang, B., Douglas-Palumberi, H., Houshyar, S., Lipschitz, D. S., Krystal, J. H., & Gelernter, J. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404376101 · Cited by 819
A FIELD STUDY OF THE SOCIOBIOLOGY OF RHESUS MONKEYS, MACACA MULATTA *
Altmann, S. A. (1962) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1962.tb13650.x · Cited by 802 · cited 1×
“Data collection included infant abuse, other mother–infant interactions (time spent in contact and frequencies of: contacts made and broken, rejections, and restrains), as well as the social and nonsocial behavior of the infants (frequencies of vocalizations, anxiety behavior, agonistic interactions with others, and s…”
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Guzman, D., Howell, B., & Sánchez, M. M. (2016) · doi:10.1002/9781118356142.ch3 · Cited by 9
Rhesus macaques form preferences for brand logos through sex and social status based advertising
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Using Behavior to Assess Primate Welfare
Lutz, C. K., & Baker, K. C. (2023) · Springer eBooks · doi:10.1007/978-3-030-82708-3_8 · Cited by 14
Molecular and Behavioral Effects of Infant Maltreatment across Generations in Rhesus MonkeysPreprint
Klengel, T., Morin, E. L., Howell, B., Bramlett, S. N., Guzman, D., Meyer, J. S., Ressler, K. J., & Sánchez, M. M. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/791152 · Cited by 8
Profiling nonhuman primate germline RNA to understand the legacy of early life stress
Morin, E. L., Garza, K. M., Aoued, H. S., Sannigrahi, S., Siebert, E. R., Howell, B., Walum, H., Sánchez, M. M., & Dias, B. G. (2021) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2501 · Cited by 6
Bogdan, R., Fitzgibbon, H., Woolverton, W. L., Bethea, C. L., Iyo, A. H., Stockmeier, C. A., Kyle, P. B., & Austin, M. C. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.08.005 · Cited by 7
“For example, both rh5-HTTLPR and gender are associated with differential hypothalamic-pituitary-adrenal axis function [19, 20].”
Wakeford, A. G. P., Morin, E. L., Bramlett, S. N., Howell, B., McCormack, K. M., Meyer, J. S., Nader, M. A., Sánchez, M. M., & Howell, L. L. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05254-8 · Cited by 7
Self-citationMethylation of OXT and OXTR genes, central oxytocin, and social behavior in female macaques
Leon, D. D., Nishitani, S., Walum, H., McCormack, K. M., Wilson, M. E., Smith, A. K., Young, L. J., & Sánchez, M. M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104856 · Cited by 7
“Focal observations were collected in real-time following published protocols (McCormack et al., 2009; Wilson et al., 2013) based on established rhesus monkey ethograms (Altmann, 1962; see ethogram in Table S1).”
MethodSelf-citationA Cross-Generational Methylomic Signature of Infant Maltreatment in Newborn Rhesus Macaques
Lardenoije, R., Smulders, M. N. C. A., Morin, E. L., Howell, B., Guzman, D., Meyer, J. S., Ressler, K. J., Sánchez, M., & Klengel, T. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.02.901 · Cited by 6
Effects of early traumatic experience on vocal expression of emotion in young female rhesus macaques
Jovanović, T., & Dario Maestripieri, A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20475 · Cited by 6
McCormack, K. M., Bramlett, S. N., Morin, E. L., Siebert, E. R., Guzman, D., Howell, B., & Sánchez, M. M. (2025) · Biology · doi:10.3390/biology14020204 · Cited by 5
“This data collection schedule is optimal to document infant MALT in rhesus monkeys, operationalized in this study as co-morbid physical abuse and rejection of the infant by the mother in the first 3 months of life, following the criteria described in previous publications [35,41,44,45,59].”
InfluentialSelf-citationDario Maestripieri, A., & Klimczuk, A. C. E. (2012) · Springer eBooks · doi:10.1007/978-1-4614-5605-6_3 · Cited by 5
“In a preliminary study, 10 abused and 10 control infants were studied during their first 6 months of life (McCormack et al. 2009).”
BackgroundEthological Case Study: Infant Abuse in Rhesus Macaques
Sánchez, M. M., McCormack, K. M., & Dario Maestripieri, A. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511711879.018 · Cited by 5
Self-citationPritchard, A. J., Capitanio, J. P., Rosso, L. A. D., McCowan, B., & Vandeleest, J. J. (2023) · Developmental Psychobiology · doi:10.1002/dev.22437 · Cited by 5
Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates
Morin, E. L., Siebert, E. R., Howell, B., Higgins, M. K., Jovanović, T., Kazama, A. M., & Sánchez, M. M. (2024) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2024.101480 · Cited by 4
“…in NHPs including rhesus macaques, where some mothers maltreat their infants during the first 3 – 6 postnatal months, resulting in increased emotional reactivity and attention to threat (McCormack et al., 2009, 2022; Morin et al., 2019; Sanchez and Pollack, 2009) similar to reports in children.”
Blomquist, G. E., Hinde, K., & Capitanio, J. P. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000493 · Cited by 4
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“…rejection and neglect of the infant during the first three months of life, resulting in pain, emotional distress, and elevations in stress hormones (Drury et al., 2017; Howell et al., 2013, 2017; Maestripieri et al., 2000; Maestripieri & Carroll, 1998; McCormack et al., 2006, 2009, 2015, 2022).”
BackgroundMethodA Bibliography Representing Spelman College Faculty Publications
Woodruff, R. W. (2013) · Atlanta University Center Robert W. Woodruff Library (Atlanta University Center Robert W. Woodruff Library)
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Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0003
Abbreviations Used for Major Brain Regions
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“…1998; Maestripieri & Carroll, 1998; Maestripieri, Higley, et al., 2006; Maestripieri, McCormack, et al., 2006; Maestripieri et al., 2000; McCormack et al., 2009; McCormack et al., 2006; McCormack et al., 2022; Sanchez, 2006) and are never exhibited by Control mothers, who showed…”
The Development of Trait Anxiety in Nonhuman Primates During the First Year of Life
Puralewski, R., Aggarwal, N., Oler, J. A., Roseboom, P. H., Parkins, L., Riedel, M. K., Boettcher, C., & Kalin, N. H. (2026) · Developmental Science · doi:10.1111/desc.70133
“…demonstrate HPA-axis activation in young rhesus monkeys (ages ranging from 2–9 months) when exposed to a stressor in the absence of their mother (Clarke 1993 ; Koch et al. 2014 ; Levine et al. 1985 ; McCormack et al. 2009 ; Sánchez et al. 2005 ; Suarez-Jimenez et al. 2013 ; Thomas et al. 1995 ).”
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(2012) · PubMed · Cited by 34
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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