Evidence for interplay between genes and parenting on infant temperament in the first year of life: monoamine oxidase A polymorphism moderates effects of maternal sensitivity on infant anger proneness
Open accessAbstract
Background: The low expression polymorphism of the MAOA gene in interaction with adverse environments (G × E) is associated with antisocial behaviour disorders. These have their origins in early life, but it is not known whether MAOA G × E occurs in infants. We therefore examined whether MAOA G × E predicts infant anger proneness, a temperamental dimension associated with later antisocial behaviour disorders. In contrast to previous studies, we examined MAOA G × E prospectively using an observational measure of a key aspect of the infant environment, maternal sensitivity, at a specified developmental time point. Methods: In a stratified epidemiological cohort recruited during pregnancy, we ascertained MAOA status (low vs. high expression alleles) from the saliva of 193 infants, and examined specific predictions to maternal report of infant temperament at 14 months from maternal sensitivity assessed at 29 weeks of age. Results: Analyses, weighted to provide general population estimates, indicated a robust interaction between MAOA status and maternal sensitivity in the prediction of infant anger proneness ( p = .003) which became stronger once possible confounders for maternal sensitivity were included in the model ( p = .0001). The interaction terms were similar in males ( p = .010) and females ( p = .016), but the effects were different as a consequence of an additional sex of infant by maternal sensitivity interaction. Conclusions: This prospective study provides the first evidence of moderation by the MAOA gene of effects of parenting on infant anger proneness, an important early risk for the development of disruptive and aggressive behaviour disorders.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
There was a gene-environment interaction: MAOA 3.5 & 4 R combined with decreased maternal sensitivity led to increased anger (p = 0.003), when adjusted for confounders (p = 0.0001).
“GxE: -> MAOA 3.5 & 4 R + decreased maternal sensitivty-> increased anger (p = 0.003), when adjusted for confounders (p = 0.0001)”
From Genetics of child aggression, a systematic review (2024) · cites this paper as Pickles [53]
The MAOA-variant results and Table 3 report the interaction with maternal sensitivity at p = .003 before adjustment and p = .0001 after adjustment. But the Allele frequencies section classifies 3.5- and 4-repeat alleles as high-activity MAOA, and the Discussion says decreasing sensitivity was associated with increasing anger only in low-activity boys; in high-activity girls it was associated with decreasing anger. The claimed direction for the 3.5- and 4-repeat group is therefore not supported. (LLM, conf=0.91)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Principles of Population Genetics.
Cormack, R. M., Hartl, D. L., & Clark, A. G. (1990) · Biometrics · doi:10.2307/2531471 · Cited by 5,283 · see citing works
Role 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 · see citing works
Beyond diathesis stress: differential susceptibility to environmental influences
Belsky, J., & Pluess, M. (2009) · Psychological Bulletin · doi:10.1037/a0017376 · Cited by 3,039 · see citing works
Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A
Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H., & van Oost, B. A. (1993) · Science · doi:10.1126/science.8211186 · Cited by 1,644 · see citing works
Studying infant temperament via the Revised Infant Behavior Questionnaire
Gartstein, M. A., & Rothbart, M. K. (2003) · Infant Behavior and Development · doi:10.1016/s0163-6383(02)00169-8 · Cited by 1,345 · see citing works
Murray, L., Fiori-Cowley, A., Hooper, R., & Cooper, P. (1996) · Child Development · doi:10.1111/j.1467-8624.1996.tb01871.x · Cited by 1,302 · see citing works
Kim-Cohen, J., Caspi, A., Taylor, A., Williams, B., Newcombe, R., Craig, I. W., & Moffitt, T. E. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001851 · Cited by 1,158 · see citing works
A functional polymorphism in the monoamine oxidase A gene promoter
Sabol, S. Z., Hu, S., & Hamer, D. (1998) · Human Genetics · doi:10.1007/s004390050816 · Cited by 1,079 · see citing works
Female and male antisocial trajectories: From childhood origins to adult outcomes
Odgers, C. L., Moffitt, T. E., Broadbent, J. M., Dickson, N. P., Hancox, R. J., Harrington, H., Poulton, R., Sears, M. R., Thomson, W. M., & Caspi, A. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000333 · Cited by 1,034 · see citing works
On the Variances of Asymptotically Normal Estimators from Complex Surveys
Binder, D. A. (1983) · International Statistical Review / Revue Internationale de Statistique · doi:10.2307/1402588 · Cited by 982 · see citing works
Neural mechanisms of genetic risk for impulsivity and violence in humans
Meyer-Lindenberg, A., Buckholtz, J. W., Kolachana, B., R. Hariri, A., Pezawas, L., Blasi, G., Wabnitz, A., Honea, R., Verchinski, B., Callicott, J. H., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511311103 · Cited by 876 · see citing works
Temperament as a unifying basis for personality and psychopathology.
Clark, L. A. (2005) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.114.4.505 · Cited by 796 · see citing works
Strategy for Investigating Interactions Between Measured Genes and Measured Environments
Moffitt, T. E., Caspi, A., & Rutter, M. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.5.473 · Cited by 784 · see citing works
Principles of Population Genetics
Cazes, M.-H., Hartl, D. L., & Clark, A. (1999) · Population · doi:10.2307/1534724 · Cited by 761 · see citing works
Deckert, J., Catalano, M., Syagailo, Y. V., Bosi, M., Okladnova, O., Di Bella, D., Nothen, M. M., Maffei, P., Franke, P., Fritze, J., et al. (1999) · Human Molecular Genetics · doi:10.1093/hmg/8.4.621 · Cited by 582 · see citing works
Child care and mother–child interaction in the first three years of life.
NICHD Early Child Care Research Network (1999) · Developmental Psychology · doi:10.1037/0012-1649.35.6.1399 · Cited by 538 · see citing works
Belsky, J., HSIEH, K.-H., & Crnic, K. A. (1998) · Development and Psychopathology · doi:10.1017/s095457949800162x · Cited by 475 · see citing works
Gender differences in emotional expressivity and self-regulation during early infancy.
Weinberg, M. K., Tronick, E. Z., Cohn, J. F., & Olson, K. L. (1999) · Developmental Psychology · doi:10.1037//0012-1649.35.1.175 · Cited by 443 · see citing works
MAOA and the neurogenetic architecture of human aggression
Buckholtz, J. W., & Meyer‐Lindenberg, A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2007.12.006 · Cited by 358 · see citing works
Gender differences in emotional expressivity and self-regulation during early infancy.
Weinberg, M. K., Tronick, E. Z., Cohn, J. F., et al. (1999) · Developmental Psychology · doi:10.1037/0012-1649.35.1.175 · Cited by 352 · see citing works
Sheese, B. E., Voelker, P., Rothbart, M. K., & Posner, M. I. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000521 · Cited by 337 · see citing works
Biological, psychological and social processes in the conduct disorders.
Hill, J. (2002) · Journal of Child Psychology and Psychiatry and Allied Disciplines · doi:10.1111/1469-7610.00007 · Cited by 329 · see citing works
Self-citationMoffitt, T. E., Caspi, A., Krueger, R. F., Magdol, L., Margolin, G., Silva, P. A., & Sydney, R. (1997) · Psychological Assessment · doi:10.1037/1040-3590.9.1.47 · Cited by 317 · see citing works
Differential susceptibility to rearing experience: the case of childcare
Pluess, M., & Belsky, J. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01992.x · Cited by 242 · see citing works
Freeman, B., Powell, J. F., Ball, D., Hill, L., Craig, I., & Plomin, R. J. (1997) · Behavior Genetics · doi:10.1023/a:1025614231190 · Cited by 236 · see citing works
Understanding Genetic Risk for Aggression: Clues From the Brain’s Response to Social Exclusion
Eisenberger, N. I., Way, B. M., Taylor, S. E., Welch, W. T., & Lieberman, M. D. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.007 · Cited by 229 · see citing works
The reliability and validity of the Infant Behavior Questionnaire-Revised
Parade, S. H., & Leerkes, E. M. (2008) · Infant Behavior and Development · doi:10.1016/j.infbeh.2008.07.009 · Cited by 189 · see citing works
Childhood Maltreatment, Subsequent Antisocial Behavior, and the Role of Monoamine Oxidase A Genotype
Huizinga, D. H., Haberstick, B. C., Smolen, A., Menard, S., Young, S. E., Corley, R. P., Stallings, M. C., Grotpeter, J. K., & Hewitt, J. K. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.12.022 · Cited by 186 · see citing works
Temperament and Parenting during the First Year of Life Predict Future Child Conduct Problems
Lahey, B. B., Hulle, C. A. V., Keenan, K. E., Rathouz, P. J., D'Onofrio, B. M., Rodgers, J. L., & Waldman, I. D. (2008) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-008-9247-3 · Cited by 160 · see citing works
Pluess, M., Velders, F. P., Belsky, J., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Jaddoe, V. W. V., Albert Hofman, D., Arp, P., Verhulst, F. C., & Tiemeier, H. W. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.10.006 · Cited by 154 · see citing works
MAOA, abuse exposure and antisocial behaviour: 30-year longitudinal study
Fergusson, D. M., Boden, J. M., Horwood, L. J., Miller, A. L., & Kennedy, M. A. (2011) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.110.086991 · Cited by 141 · see citing works
Sharp, H. M., Pickles, A. R., Meaney, M. J., Marshall, K. H., Tibu, F., & Hill, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045446 · Cited by 140 · see citing works
Self-citationÅslund, C., Nordquist, N., Comasco, E., Leppert, J., Oreland, L., & Nilsson, K. W. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9356-y · Cited by 126 · see citing works
Multiple Determinants of Externalizing Behavior in 5-Year-Olds: A Longitudinal Model
Smeekens, S., Riksen‐Walraven, J. M., & van Bakel, H. J. A. (2007) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-006-9095-y · Cited by 124 · see citing works
Enoch, M., Steer, C. D., Newman, T. K., Gibson, N. P. S. J., & Goldman, D. A. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00535.x · Cited by 104 · see citing works
Beach, S. R. H., Brody, G. H., Gunter, T. D., Packer, H., Wernett, P., & Philibert, R. A. (2010) · Journal of Family Psychology · doi:10.1037/a0018074 · Cited by 100 · see citing works
Moderating role of the MAOA genotype in antisocial behaviour
Fergusson, D. M., Boden, J. M., Horwood, L. J., Miller, A. L., & Kennedy, M. A. (2012) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.111.093328 · Cited by 96 · see citing works
A longitudinal analysis of anger and inhibitory control in twins from 12 to 36 months of age
Gagne, J. R., & Goldsmith, H. H. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2010.00969.x · Cited by 95 · see citing works
Child Abuse and Neglect, MAOA, and Mental Health Outcomes: A Prospective Examination
Nikulina, V., Widom, C. S., & Brzustowicz, L. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.008 · Cited by 76 · see citing works
Warren, S. L., & Simmens, S. J. (2005) · Infant Mental Health Journal · doi:10.1002/imhj.20034 · Cited by 61 · see citing works
No evidence for interaction between MAOA and childhood adversity for antisocial behavior
Prichard, Z. M., Mackinnon, A. J., Jorm, A. F., & Easteal, S. (2007) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30581 · Cited by 55 · see citing works
Sheese, B. E., Voelker, P., Posner, M. I., & Rothbart, M. K. (2009) · Cognitive Neuropsychiatry · doi:10.1080/13546800902844064 · Cited by 51 · see citing works
Anger, Preoccupied Attachment, and Domain Disorganization in Borderline Personality Disorder
Morse, J. Q., Hill, J., Pilkonis, P. A., Yaggi, K. E., Broyden, N., Stepp, S. D., Reed, L. I., & Feske, U. (2009) · Journal of Personality Disorders · doi:10.1521/pedi.2009.23.3.240 · Cited by 45 · see citing works
Self-citationHill, J., Breen, G. D., Quinn, J. P., Tibu, F., Sharp, H. M., & Pickles, A. R. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12033 · Cited by 42 · see citing works
Self-citationLehmann, A. S., Haas, D. M., McCormick, C. L., et al. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.12.013 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Genetics of aggressive behavior: An overview
Veroude, K., Zhang‐James, Y., Fernàndez‐Castillo, N., Bakker, M. J., Cormand, B., & Faraone, S. V. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32364 · Cited by 147 · see citing works
Kolla, N. J., & Bortolato, M. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101875 · Cited by 138 · see citing works
Aggressive behavior in humans: Genes and pathways identified through association studies
Fernàndez‐Castillo, N., & Cormand, B. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32419 · Cited by 87 · see citing works
Zhang, W., Cao, C., Wang, M., Ji, L., & Cao, Y. (2016) · Journal of Youth and Adolescence · doi:10.1007/s10964-016-0442-1 · Cited by 50 · see citing works
Genetics of child aggression, a systematic review
Koyama, E., Kant, T., Takata, A., Kennedy, J. L., & Zai, C. C. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02870-7 · Cited by 33 · see citing works
- Authors
- Pickles, A., Hill, J., Breen, G., Quinn, J., Abbott, K., Jones, H., & Sharp, H.
- Affiliations
- King's College London (GB)
- University of Manchester (GB)
- University of Liverpool (GB)
- Corresponding author
- Hill, Jonathan
- Venue
- Journal of Child Psychology and Psychiatry
- Publisher
- Wiley
- Published
- 2013-06-06
- Volume
- 54
- Issue
- 12
- Pages
- 1308-1317
- ISSN
- 0021-9630 (ISSN-L)
- 1469-7610
- OpenAlex
- W2111052531
- Cited by
- 47
- References
- 45
- Citations by year
- 2024: 2 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 6 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 11 · 2015: 6 · 2014: 4 · 2013: 2
- FWCI
- 8.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Child Psychology and Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- CentAUR (University of Reading) (acceptedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Funders
- Medical Research Council
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Clinical Psychology › Psychopathy, Forensic Psychiatry, Sexual Offending
- Keywords
- monoamine oxidase A, gene-environment interaction, maternal sensitivity, parenting, infant temperament, antisocial behavior, sex differences, first year of life
- MeSH terms
- Adolescent, Adult, Alleles, Anger, England, Female, Genotype, Humans, Infant, Male, Middle Aged, Monoamine Oxidase, Mother-Child Relations, Mothers, Polymorphism, Genetic, Promoter Regions, Genetic, Prospective Studies, Sex Factors, Temperament, Parenting, Genetic Predisposition to Disease, Young Adult, Gene-Environment Interaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review