Sex differences in structural brain asymmetry predict overt aggression in early adolescents

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 4, 2014, Pages 553-560

  Visser, Troy A W ^a   Ohan, Jeneva L ^a   Whittle, Sarah ^b,c   Yücel, Murat ^b,c   Simmons, Julian G ^b,d   Allen, Nicholas B ^b,d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aggression; Anterior cingulate; Brain asymmetry; Orbitofrontal cortex; Sex difference

Indexed keywords

ADOLESCENT; AGGRESSION; ANALYSIS OF VARIANCE; ANATOMY AND HISTOLOGY; BRAIN; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; IMAGE PROCESSING; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREDICTIVE VALUE; SEXUAL DEVELOPMENT; SOCIOECONOMICS;

ADOLESCENT; AGGRESSION; ANALYSIS OF VARIANCE; BRAIN; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; PREDICTIVE VALUE OF TESTS; SEX CHARACTERISTICS; SOCIOECONOMIC FACTORS;

EID: 84898835318     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst013     Document Type: Article

References (83)

1. Archer, J. (2004). Sex differences in aggression in real-world settings: a meta-analytic review. Review of General Psychology, 8, 291-322.
2. Armstrong, E., Schleicher, A., Omran, H., Curtis, M., Zilles, K. (1995). The ontogeny of human gyrification. Cerebral Cortex, 5, 56-63.
3. Bandura, A. (1973). Aggression: A Social Learning Analysis. Englewood Cliffs, NJ: Prentice-Hall.
4. Bilder, R.M., Wu, H., Bogerts, B., et al. (1999). Cerebral volume asymmetries in schizophrenia and mood disorders: a quantitative magnetic resonance imaging study. International Journal of Psychophysiology, 34, 197-205.
5. Birbaumer, N., Veit, R., Lotze, M., et al. (2005). Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. Archives of General Psychiatry, 62, 799-805.
6. Bjorkqvist, L., Osterman, K., Kaukiainen, A. (1992). The development of direct and indirect aggressive strategies in males and females. In: Bjorkqvist, K., Niemelae, P., editors. Of Mice and Women: Aspects of Female Aggression. San Diego: Academic Press, pp. 51-64.
7. Boes, A.D., Tranel, D., Anderson, S.W., Nopoulos, P. (2008). Right anterior cingulate: a neuroanatomical correlate of aggression and defiance in boys. Behavioral Neuroscience, 122, 677-84.
8. Bufkin, J.L., Luttrell, V.R. (2005). Neuroimaging studies of aggressive and violent behavior: current findings and implications for criminology and criminal justice. Trauma, Violence, & Abuse, 6, 176-91.
9. Carter, C.S., Macdonald, A.M., Botvinick, M., et al. (2000). Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National Academy of Sciences of the United States of America, 97, 1944-8.
10. Chanen, A.M., Velakoulis, D., Carison, K., et al. (2008). Orbitofrontal, amygdala and hippocampal volumes in teenagers with first-presentation borderline personality disorder. Psychiatry Research, 163, 116-25.
11. Chesterman, L.P., Taylor, P.J., Cox, T., Hill, M. (1994). Multiple measures of cerebral state in dangerous mentally disordered inpatients. Criminal Behaviour and Mental Health, 4, 228-39.
12. Coccaro, E.F., McCloskey, M., Fitzgerald, D.A., Phan, K.L. (2007). Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biological Psychiatry, 62, 168-78.
13. Crick, N.R. (1996). The role of overt aggression, relational aggression, and prosocial behavior in children's future social adjustment. Child Development, 67, 2317-27.
14. Crick, N.R., Grotpeter, J.K. (1995). Relational aggression, gender, and social-psychological adjustment. Child Development, 66, 710-22.
15. Critchley, H.D., Simmons, A., Daly, E.M., et al. (2000). Prefrontal and medial temporal correlates of repetitive violence to self and others. Biological Psychiatry, 15, 928-34.
16. Davidson, R.J., Putnam, K.M., Larson, C.L. (2000). Dysfunction in the neural circuitry of emotion regulation-a possible prelude to violence. Science, 289, 591-4.
17. Dollard, J., Doob, L., Miller, N., Mowrer, O., Sears, R. (1939). Frustration and Aggression. New Haven, CT: Yale University Press.
18. Dougherty, D.D., Rauch, S.L., Deckersbach, T., et al. (2004). Ventromedial prefrontal cortex and amygdala dysfunction during an anger induction positron emission tomography study in patients with major depressive disorder with anger attacks. Archives of General Psychiatry, 61, 795-804.
19. Driessen, M., Herrmann, J., Stahl, K., et al. (2000). Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Archives of General Psychiatry, 57, 1115-22.
20. Eisenberger, N.I., Way, B.M., Taylor, S.E., Welch, W.T., Lieberman, M.D. (2007). Understanding genetic risk for aggression: clues from the brain's response to social exclusion. Biological Psychiatry, 35, 1601-12.
21. Ellis, L.K., Rothbart, M.K. (2001). Revision of the Early Adolescent Temperament Questionnaire. Poster presented at the Biennial Meeting of the Society for Research in Child Development, Minneapolis, MN.
22. Fairchild, G., Passamonti, L., Hurford, G., et al. (2011). Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. American Journal of Psychiatry, 168, 624-33.
23. Farrell, A.D., Sullivan, T.N., Esposito, L.E., Meyer, A.L., Valois, R.F. (2005). A latent growth curve analysis of the structure of aggression, drug use, and delinquent behaviours and their interrelations over time in urban and rural adolescents. Journal of Research on Adolescence, 15, 179-204.
24. Forbes, E.E., Shaw, D.S., Fox, N.A., Cohn, J.F., Silk, J.S., Kovacs, M. (2006). Maternal depression, child frontal asymmetry, and child affective behavior as factors in child behavior problems. Journal of Child Psychology and Psychiatry, 47, 79-87.
25. Fornito, A., Whittle, S., Wood, S.J., Velakoulis, D., Pantelis, C., Yücel, M. (2006). The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex. Neuroimage, 33, 843-54.
26. Fornito, A., Wood, S.J., Whittle, S., et al. (2008). Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: associations with cortical thickness, surface area, volume, and sulcal depth. Human Brain Mapping, 29, 222-36.
27. Foundas, A.L., Leonard, C.M., Gilmore, R.L., Fennell, E.B., Heilman, K.M. (1996). Pars triangularis asymmetry and language dominance. Proceedings of the National Academy of Sciences of the United States of America, 93, 719-22.
28. Giedd, J.N., Blumenthal, J., Jeffries, N.O., et al. (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neuroscience, 2, 861-3.
29. Goyer, P.F., Andreason, P.J., Semple, W.E., et al. (1994). Positron emission tomography and personality disorders. Neuropsychopharmacology, 10, 21-8.
30. Grafman, J., Schwab, K., Warden, D., Pridgen, A., Brown, H.R., Salazar, A.M. (1996). Frontal lobe injuries, violence, and aggression: a report of the Vietnam Head Injury Study. Neurology, 46, 1231-8.
31. Hess, N.H., Hagen, E.H. (2006). Sex differences in informational aggression: psychological evidence from young adults. Evolution and Human Behavior, 27, 231-45.
32. Huebner, T., Voet, T.D., Marx, I., et al. (2008). Morphometic brain abnormalities in boys with conduct disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 47, 540-7.
33. Jenkinson, M., Smith, S.M. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143-56.
34. Juárez, M., Kiehl, K.A., Calhoun, V.D. (2013). Intrinsic limbic and paralimbic networks are associated with criminal psychopathy. Human Brain Mapping, 34(8), 1921-30.
35. Juhasz, C., Behen, M.E., Muzik, O., Chugani, D.C., Chugani, H.T. (2001). Bilateral medial prefrontal and temporal neocortical hypometabolism in children with epilepsy and aggression. Epilepsia, 42, 991-1001.
36. Karriker-Jaffe, K.J., Foshee, V.A., Ennett, S.T., Suchindran, C. (2008). The development of aggression during adolescence: sex differences in trajectories of physical and social aggression among youth in rural areas. Journal of Abnormal Child Psychology, 36, 1227-36.
37. Keshavan, M.S., Dick, E., Mankowski, I., et al. (2002). Decreased left amygdala and hippocampal volumes in young offspring at risk for schizophrenia. Schizophrenia Research, 58, 173-83.
38. Laakso, M.P., Vaurio, O., Koivisto, E., et al. (2001). Psychopathy and the posterior hippocampus. Behavioral Brain Research, 118, 187-93.
39. Lenroot, R.K., Giedd, J.N. (2006). Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neuroscience and Biobehavioral Reviews, 30, 718-29.
40. Little, T., Henrich, C., Jones, S., Hawley, P. (2003). Dientangling the "whys" and the "whats" of aggressive behaviour. International Journal of Behavioral Development, 27, 122-33.
41. Loeber, R., Hay, D.F. (1997). Key issues in the development of aggression and violence from childhood to early adulthood. Annual Review of Psychology, 48, 371-410.
42. Lorenz, K.Z. (1958). The evolution of behavior. Scientific American, 199, 67-78.
43. Luders, E., Rex, D.E., Narr, K.L., et al. (2003). Relationships between sulcal asymmetries and corpus callosum size: gender and handedness effects. Cerebral Cortex, 23, 1084-93.
44. Meyer-Lindenberg, A., Buckholtz, J.W., Kolachana, B., et al. (2006). Neural mechanisms of genetic risk for impulsivity and violence in humans. Proceedings of the National Academy of Sciences of the United States of America, 103, 6269-74.
45. Minzenberg, M.J., Fan, J., New, A.S., Tang, C.Y., Siever, L.J. (2007). Front-limbic dysfunction in response to facial emotion in borderline personality disorder: an event-related fMRI study. Psychiatry Research, 155, 231-43.
46. Motzkin, J.C., Newman, J.P., Kiehl, K.A., Koenigs, M. (2011). Reduced prefrontal connectivity in psychopathy. Journal of Neuroscience, 31, 17348-57.
47. Nunes, P.M., Wenzel, A., Borges, K.T., Porto, C.R., Caminha, R.M., de Oliveira, I.R. (2009). Volumes of the hippocampus and amygdala in patients with borderline personality disorder: a meta-analysis. Journal of Personality Disorders, 23, 333-45.
48. Oldfield, R.C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97-113.
49. Orvaschel, H., Lewinsohn, P.M., Seeley, J.R. (1995). Continuity of psychopathology in a community sample of adolescents. Journal of the American Academy of Child and Adolescent Psychiatry, 34, 1525-35.
50. Pepler, D.J., Craig, W.M. (2005). Aggressive girls on troubled trajectories: a developmental perspective. In: Pepler, D.J., editor. Development and Treatment of Girlhood Aggression. Mahwah, NJ: Erlbaum, pp. 3-28.
51. Powell, H.W.R., Parker, G.J.M., Alexander, D.C., et al. (2006). Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage, 32, 388-99.
52. Prinstein, M.J., Boergers, J., Vernberg, E.M. (2001). Overt and relational aggression in adolescents: psychological adjustment of aggressors and victims. Journal of the American Academy of Child and Adolescent Psychiatry, 30, 479-91.
53. Raine, A. (2008). From genes to brain to antisocial behaviour. Current Directions in Psychological Science, 17, 323-8.
54. Raine, A., Buchsbaum, M., LaCasse, L. (1997). Brain abnormalities in murderers indicated by positron emission tomography. Biological Psychiatry, 42, 495-508.
55. Raine, A., Ishikawa, S.S., Arce, E., et al. (2004). Hippocampal structural asymmetry in unsuccessful psychopaths. Biological Psychiatry, 55, 185-91.
56. Raine, A., Meloy, J.R., Bihrle, S., Stoddard, J., LaCasse, L., Buchsbaum, M.S. (1998). Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behavioral Sciences & the Law, 16, 319-32.
57. Riffkin, J., Yücel, M., Maruff, P., et al. (2005). A manual and automated MRI study of anterior cingulate and orbito-frontal cortices, and caudate nucleus in obsessivecompulsive disorder: comparison with healthy controls and patients with schizophrenia. Psychiatry Research, 138, 99-113.
58. Rogers, L.J. (2002). Lateralization in vertebrates: its early evolution, general pattern, and development. Advances in the Study of Behavior, 31, 107-61.
59. Salmivalli, C., Kaukiainen, A., Lagerspetz, K. (2000). Aggression and sociometric status among peers: do gender and type of aggression matter? Scandinavian Journal of Psychology, 41, 17-24.
60. Sanders, G.S., Gallup, G.G., Heinsen, H., Hof, P.R., Schmitz, C. (2002). Cognitive deficits, schizophrenia, and the anterior cingulate cortex. Trends in Cognitive Sciences, 6, 190-2.
61. Schmahla, C.G., Vermettenb, E., Elzingac, B.M., Bremnerde, J.D. (2003). Magnetic resonance imaging of hippocampal and amygdala volume in women with childhood abuse and borderline personality disorder. Psychiatry Research, 122, 193-8.
62. Smith, S.M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143-55.
63. Soderstrom, H., Tullberg, M., Wikkelso, C., Ekholm, S., Forsman, A. (2000). Reduced regional cerebral blood flow in non-psychotic violent offenders. Psychiatry Research, 98, 29-41.
64. 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, 335-42.
65. Toga, A.W., Thompson, P.M. (2003). Mapping brain asymmetry. Nature Reviews Neuroscience, 4, 37-8.
66. Tolan, P.H., Gorman-Smith, D., Loeber, R. (2000). Developmental timing of onsets of disruptive behaviors and later delinquency of inner-city youth. Journal of Child and Family Studies, 9, 203-30.
67. Tomada, G., Schneider, B.H. (1997). Relational aggression, gender, and peer acceptance: invariance across culture, stability over time, and concordance among informants. Developmental Psychobiology, 33, 601-9.
68. Tonkonogy, J.M. (1991). Violence and temporal lobe lesion: Head CT and MRI data. Journal of Neuropsychiatry and Clinical Neurosciences, 3, 189-96.
69. Trewin, D. (2001). Census of Population and Housing: Socio-Economic Indexes for area's (SEIFA). Canberra: Australian Bureau of Statistics.
70. van Elst, L.T., Hesslinger, B., Thiel, T., et al. (2003). Frontolimbic brain abnormalities in patients with borderline personality disorder: a volumetric magnetic resonance imaging study. Biological Psychiatry, 54, 163-71.
71. Vazsonyi, A.T., Keiley, M.K. (2007). Normative developmental trajectories of aggressive behaviors in African American, American Indian, Asian American, Caucasian, and Hispanic children and early adolescents. Journal of Abnormal Child Psychology, 35, 1047-62.
72. Velakoulis, D., Pantelis, C., McGorry, P.D., et al. (1999). Hippocampal volume in first-episode psychoses and chronic schizophrenia: a high-resolution magnetic resonance imaging study. Archives of General Psychiatry, 56, 133-41.
73. Velakoulis, D., Wood, S.J., Wong, M.T., et al. (2006). Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, Erst-episode psychosis, and ultra-high-risk individuals. Archives of General Psychiatry, 63, 139-49.
74. Walhovd, K.B., Tames, C.K., Ostby, Y., Due-Tønnessen, P., Fjell, A.M. (2012). Normal variation in behavioural adjustment relates to regional differences in cortical thickness in children. European Child & Adolescent Psychiatry, 21, 133-40.
75. Watson, C., Andermann, F., Gloor, P., et al. (1992). Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic-resonance-imaging. Neurology, 42, 1743-50.
76. Weinberger, D.R., McClure, R.K. (2002). Neurotoxicity, neuroplasticity, and magnetic resonance imaging morphometry: what is happening in the schizophrenic brain? Archives of General Psychiatry, 59, 533-58.
77. Whittle, S., Yap, M.B.H., Yücel, M., et al. (2008). Prefrontal and amygdala volumes are related to adolescents' affective behaviors during parent-adolescent interactions. Proceedings of the National Academy of Sciences of the United States of America, 105, 3652-7.
78. Woermann, F.G., van Elst, L.T., Koepp, M.J., et al. (2000). Reduction of frontal neocortical grey matter associated with affective aggression in patients with temporal lobe epilepsy: an objective voxel by voxel analysis of automatically segmented MRI. Journal of Neurology, Neurosurgery, and Psychiatry, 68, 162-9.
79. Yang, Y., Raine, A. (2009). Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Research, 174, 81-8.
80. Yücel, M., Stuart, G.W., Maruff, P., et al. (2001). Hemispheric and gender-related differences in the gross morphology of the anterior cingulate/paracingulate cortex in normal volunteers: an MRI morphometric study. Cerebral Cortex, 11, 17-25.
81. Yücel, M., Stuart, G.W., Maruff, P., et al. (2002). Paracingulate morphologic differences in males with established schizophrenia: a magnetic resonance imaging morphometric study. Biological Psychiatry, 52, 15-23.
82. Zhang, Y., Brady, M., Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Transactions on Medical Imaging, 20, 45-57.
83. Zilles, K., Dabringhaus, A., Geyer, S., et al. (1996). Structural asymmetries in the human forebrain and the forebrain of non-human primates and rats. Neuroscience and Biobehavioral Reviews, 20, 593-605.