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Neural mediators of the intergenerational transmission of family aggression

Published online by Cambridge University Press:  15 June 2015

Darby Saxbe*
Affiliation:
University of Southern California
Larissa Borofsky Del Piero
Affiliation:
University of Southern California
Mary Helen Immordino-Yang
Affiliation:
University of Southern California
Jonas Todd Kaplan
Affiliation:
University of Southern California
Gayla Margolin
Affiliation:
University of Southern California
*
Address correspondence and reprint requests to: Darby Saxbe, Department of Psychology, SGM 501, 3620 McClintock Avenue, University of Southern California, Los Angeles, CA 90089; E-mail: dsaxbe@usc.edu.

Abstract

Youth exposed to family aggression may become more aggressive themselves, but the mechanisms of intergenerational transmission are understudied. In a longitudinal study, we found that adolescents’ reduced neural activation when rating their parents’ emotions, assessed via magnetic resonance imaging, mediated the association between parents’ past aggression and adolescents’ subsequent aggressive behavior toward parents. A subsample of 21 youth, drawn from the larger study, underwent magnetic resonance imaging scanning proximate to the second of two assessments of the family environment. At Time 1 (when youth were on average 15.51 years old) we measured parents’ aggressive marital and parent–child conflict behaviors, and at Time 2 (≈2 years later), we measured youth aggression directed toward parents. Youth from more aggressive families showed relatively less activation to parent stimuli in brain areas associated with salience and socioemotional processing, including the insula and limbic structures. Activation patterns in these same areas were also associated with youths’ subsequent parent-directed aggression. The association between parents’ aggression and youths’ subsequent parent-directed aggression was statistically mediated by signal change coefficients in the insula, right amygdala, thalamus, and putamen. These signal change coefficients were also positively associated with scores on a mentalizing measure. Hypoarousal of the emotional brain to family stimuli may support the intergenerational transmission of family aggression.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2015 

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References

Adolphs, R. (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences, 1191, 4261.Google Scholar
Adolphs, R., Tranel, D., Hamann, S., Young, A., Calder, A., Phelps, E., et al. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37, 11111117. doi:10.1016/S0028-3932(99)00039-1 Google Scholar
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “Reading the Mind in the Eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, 42, 241251. doi:10.1111/1469-7610.00715 Google Scholar
Barrett, L. F. (2006). Solving the emotion paradox: Categorization and the experience of emotion. Personality and Social Psychology Review, 10, 2046. doi:10.1207/s15327957pspr1001_2 Google Scholar
Barrett, L. F., Mesquita, B., Ochsner, K. N., & Gross, J. J. (2007). The experience of emotion. Annual Review of Psychology, 58, 373.Google Scholar
Blakemore, S. J., & Mills, K. L. (2014). Is adolescence a sensitive period for sociocultural processing? Annual Review of Psychology, 65, 187207.Google Scholar
Brown, C. L., Oudekerk, B. A., Szwedo, D. E., & Allen, J. P. (2013). Inter-parent aggression as a precursor to disengagement coping in emerging adulthood: The buffering role of friendship competence. Social Development, 22, 683700.Google Scholar
Cappell, C., & Heiner, R. B. (1990). The intergenerational transmission of family aggression. Journal of Family Violence, 5, 135152. doi:10.1007/BF00978516 Google Scholar
Chang, L., Schwartz, D., Dodge, K. A., & McBride-Chang, C. (2003). Harsh parenting in relation to child emotion regulation and aggression. Journal of Family Psychology, 17, 598606. http://dx.doi.org/10.1037/0893-3200.17.4.598 Google Scholar
Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189195. doi:10.1038/nn1176 Google Scholar
Damasio, A. R. (1994). Descartes’ error: Emotion, rationality and the human brain (p. 352). New York: Putnam.Google Scholar
Damasio, A., & Carvalho, G.B. (2013). The nature of feelings: Evolutionary and neurobiological origins. Nature Reviews Neuroscience, 14, 143152.Google Scholar
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., et al. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286293. doi:10.1016/j.biopsych.2011.10.021 Google Scholar
Denham, S. A., Blair, K. A., DeMulder, E., Levitas, J., Sawyer, K., Auerbach–Major, S., et al. (2003). Preschool emotional competence: Pathway to social competence?. Child Development, 74, 238256. doi:10.1111/1467-8624.00533 Google Scholar
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2010). Reduced electrodermal fear conditioning from ages 3 to 8 years is associated with aggressive behavior at age 8 years. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 550558. doi:10.1111/j.1469-7610.2009.02176.x Google Scholar
Gunnar, M. R., & Donzella, B. (2002). Social regulation of cortisol levels in early human development. Psychoneuroendocrinology, 27, 199220.Google Scholar
Hooker, C. I., Verosky, S. C., Germine, L. T., Knight, R. T., & D'Esposito, M. (2008). Mentalizing about emotion and its relationship to empathy. Social Cognitive and Affective Neuroscience, 3, 204217. doi:10.1093/scan/nsn019 Google Scholar
Immordino-Yang, M. H., McColl, A., Damasio, H., & Damasio, A. (2009). Neural correlates of admiration and compassion. Proceeding of the National Association of Sciences, 106, 80218026. doi:10.1073/pnas.0810363106 Google Scholar
Immordino-Yang, M. H., & Singh, V. (2013). Hippocampal contributions to the processing of social emotions. Human Brain Mapping, 34, 945955.Google Scholar
Immordino-Yang, M. H., Yang, X. F., & Damasio, H. (2014). Correlations between social–emotional feelings and anterior insula activity are independent from visceral states but influenced by culture. Frontiers in Human Neuroscience, 8, 728. doi:10.3389/fnhum.2014.00728 Google Scholar
Jackson, P. L., Meltzoff, A. N., & Decety, J. (2005). How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage, 24, 771779.Google Scholar
Jones, A., Laurens, K., Herba, C., Barker, G., & Viding, E. (2009). Amygdala hypoactivity to fearful faces in boys with conduct problems and callous–unemotional traits. American Journal of Psychiatry, 166, 95102.Google Scholar
Kim, S., Fonagy, P., Allen, J., & Strathearn, L. (2014). Mothers’ unresolved trauma blunts amygdala response to infant distress. Social Neuroscience. Advance online publication. doi:10.1080/17470919.2014.896287 Google Scholar
Lindquist, K. A., Wager, T. D., Kober, H., Bliss-Moreau, E., & Barrett, L. F. (2012). The brain basis of emotion: A meta-analytic review. Behavioral and Brain Sciences, 35, 121143.Google Scholar
Margolin, G., & Baucom, B. R. (2014). Adolescents’ aggression to parents: Longitudinal links with parents’ physical aggression. Journal of Adolescent Health. Advance online publication. http://dx.doi.org/10.1016/j.jadohealth.2014.05.008 CrossRefGoogle ScholarPubMed
Margolin, G., John, R. S., & Foo, L. (1998). Interactive and unique risk factors for husbands’ emotional and physical abuse of their wives. Journal of Family Violence, 13, 315344. doi:10.1023/A:1022880518367 Google Scholar
Margolin, G., Vickerman, K. A., Oliver, P. H., & Gordis, E. B. (2010). Violence exposure in multiple interpersonal domains: Cumulative and differential effects. Journal of Adolescent Health, 47, 198205. doi:10.1016/j.jadohealth.2010.01.020 Google Scholar
Mathiak, K., & Weber, R. (2006). Toward brain correlates of natural behavior: fMRI during violent video games. Human Brain Mapping, 27, 948956. doi:10.1002/hbm.20234 Google Scholar
McNeal, C., & Amato, P. R. (1998). Parents’ marital violence: Long-term consequences for children. Journal of Family Issues, 19, 123139. doi:10.1177/019251398019002001 CrossRefGoogle Scholar
Michael, K. C., Torres, A., & Seemann, E. A. (2007). Adolescents’ health habits, coping styles and self-concept are predicted by exposure to interparental conflict. Journal of Divorce & Remarriage, 48, 155174.CrossRefGoogle Scholar
Miller, P.A., & Eisenberg, N. (1988). The relation of empathy to aggressive and externalizing/antisocial behavior. Psychological Bulletin, 103, 324344. http://dx.doi.org/10.1037//0033-2909.103.3.324 Google Scholar
Moses-Kolko, E., Horner, M. S., Phillips, M., Hipwell, A., & Swain, J. (2014). In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. Journal of Neuroendocrinology. Advance online publication. 10.1111/jne.12183 Google Scholar
Nummenmaa, L., Hirvonen, J., Parkkola, R., & Hietanen, J. K. (2008). Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. NeuroImage, 43, 571580. doi:10.1016/j.neuroimage.2008.08.014 Google Scholar
Olsavsky, A. K., Telzer, E. H., Shapiro, M., Humphreys, K. L., Flannery, J., Goff, B., et al. (2013). Indiscriminate amygdala response to mothers and strangers after early maternal deprivation. Biological Psychiatry, 74, 853860. doi:10.1016/j.biopsych.2013.05.025 Google Scholar
Patterson, G. R. (1982). Coercive family process (Vol. 3). New York: Castalia.Google Scholar
Pessoa, L., & Adolphs, R. (2010). Emotion processing and the amygdala: From a “low road” to “many roads” of evaluating biological significance. Nature Reviews. Neuroscience, 11, 773783. doi:10.1038/nrn2920 Google Scholar
Pine, D. S., Mogg, K., Bradley, B. P., Montgomery, L., Monk, C. S., McClure, E., et al. (2005). Attention bias to threat in maltreated children: implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry, 162, 291296.Google Scholar
Pollak, S. D. (2005). Early adversity and mechanisms of plasticity: Integrating affective neuroscience with developmental approaches to psychopathology. Development and Psychopathology, 17, 735752. doi:10.1017/S0954579405050352 Google Scholar
Preacher, K. J., & Hayes, A. F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, and Computers, 36, 717731. doi:10.3758/BF03206553 Google Scholar
Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879891.Google Scholar
Preston, S. D., & deWaal, F. B. M. (2002). Empathy: Its ultimate and proximate bases. Behavioral & Brain Sciences, 25, 172.CrossRefGoogle ScholarPubMed
Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 296301.Google Scholar
Rilling, J. K. (2013). The neural and hormonal bases of human parental care. Neuropsychologia, 51, 731747. doi:10.1016/j.neuropsychologia.2012.12.017 Google Scholar
Russell, J. A., & Barrett, L. F. (1999). Core affect, prototypical emotional episodes, and other things called “emotion”: Dissecting the elephant. Journal of Personality and Social Psychology, 76, 805. http://dx.doi.org/10.1037/0022-3514.76.5.805 Google Scholar
Saxbe, D. E., Margolin, G., Spies Shapiro, L. A., & Baucom, B. R. (2012). Does dampened physiological reactivity protect youth in aggressive family environments? Child Development, 83, 821830. doi:10.1111/j.1467-8624.2012.01752.x Google Scholar
Seiffge-Krenke, I. (2011). Coping with relationship stressors: A decade review. Journal of Research on Adolescence, 21, 196210. doi:10.1111/j.1532-7795.2010.00723.x Google Scholar
Seo, D., Tsou, K. A., Ansell, E. B., Potenza, M. N., & Sinha, R. (2013). Cumulative adversity sensitizes neural response to acute stress: Association with health symptoms. Neuropsychopharmacology, 39, 670680.Google Scholar
Seth, A. K. (2013). Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences, 17, 565573.Google Scholar
Shackman, J. E., Fatani, S., Camras, L. A., Berkowitz, M. J., Bachorowski, J.-A., & Pollak, S. D. (2010). Emotion expression among abusive mothers is associated with their children's emotion processing and problem behaviours. Cognition & Emotion, 24, 14211430. doi:10.1080/02699930903399376 CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Vitacco, M. J., Graf, A. R., Gostisha, A. J., Merz, J. L., & Zahn-Waxler, C. (2009). Neurobiology of empathy and callousness: Implications for the development of antisocial behavior. Behavioral Sciences & the Law, 27, 137171.Google Scholar
Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13, 334340. doi:10.1016/j.tics.2009.05.001 Google Scholar
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 11571162. doi:10.1126/science.1093535 Google Scholar
Smith, C. A., Ireland, T. O., Park, A., Elwyn, L., & Thornberry, T. P. (2011). Intergenerational continuities and discontinuities in intimate partner violence: A two-generational prospective study. Journal of Interpersonal Violence, 26, 37203752. doi:10.1177/0886260511403751 Google Scholar
Sterzer, P., Stadler, C., Poustka, F., & Kleinschmidt, A. (2007). A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. NeuroImage, 37, 335342. doi:10.1016/j.neuroimage.2007.04.043 Google Scholar
Straus, M. A., Hamby, S. L., Finkelhor, D., Moore, D. W., & Runyan, D. (1998). Identification of child maltreatment with the parent–child conflict tactics scales: Development and psychometric data for a national sample of American parents. Child Abuse & Neglect, 22, 249270. doi:10.1016/S0145-2134(97)00174-9 Google Scholar
Susman, E. J. (2006). Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis. Neuroscience & Biobehavioral Reviews, 30, 376389.Google Scholar
Taylor, S. E., Eisenberger, N. I., Saxbe, D., Lehman, B. J., & Lieberman, M. D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry, 60, 296301.Google Scholar
Tottenham, N., Shapiro, M., Telzer, E. H., & Humphreys, K. L. (2012). Amygdala response to mother. Developmental Science, 15, 307319. doi:10.1111/j.1467-7687.2011.01128.x Google Scholar
Van Overwalle, F., & Baetens, K. (2009) Understanding others’ actions and goals by mirror and mentalizing systems: A meta-analysis. NeuroImage, 48, 564584.Google Scholar
Wager, T. D., & Nichols, T. E. (2003). Optimization of experimental design in fMRI: A general framewor using a genetic algorithm. NeuroImage, 18, 293309.Google Scholar
Whittle, S., Yücel, M., Forbes, E. E., Davey, C. G., Harding, I. H., Sheeber, L., et al. (2012). Adolescents’ depressive symptoms moderate neural responses to their mothers’ positive behavior. Social Cognitive and Affective Neuroscience, 7, 2334.Google Scholar