Although callous-unemotional (CU) traits have been associated with amygdala hypoactivity, it is unclear whether such traits are associated with amygdala structure. This study examines the relationship between amygdala structure and CU traits and considers sex differences in hemisphere-related asymmetries in this relationship. In this brain imaging study of children (n = 272), a significant sex × hemisphere × CU traits interaction was observed. Females with high CU traits and males with low CU exhibited a rightward exaggerated amygdala volume asymmetry, whereas females with low CU traits and males with high CU traits did not. Findings may reflect sex-related influences related to CU traits and amygdala volume and are broadly consistent with a neurodevelopment perspective on psychopathic-like traits in children.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). In Diagnostic and statistical manual of mental disorders (4th ed.).
2.
BarryC. T.FrickP. J.DeshazoT. M.McCoyM. G.EllisM.LoneyB. R. (2000). The importance of callous-unemotional traits for extending the concept of psychopathy to children. Journal of Abnormal Psychology, 109(2), 335–340. https://doi.org/10.1037/0021-843X.109.2.335
3.
BlakemoreS. J.BurnettS.DahlR. E. (2010). The role of puberty in the developing adolescent brain. Human Brain Mapping, 6, 926–933. https://doi.org/10.1002/hbm.21052
4.
BolhuisK.VidingE.MuetzelR. L.El MarrounH.KocevskaD.WhiteT.TiemeierH.CecilC. A. M. (2019). Neural profile of callous traits in children: A population-based neuroimaging study. Biological Psychiatry, 65(5), 399–407. https://doi.org/10.1016/j.biopsych.2018.10.015
5.
BramenJ. E.HranilovichJ. A.DahlR. E.ForbesE. E.ChenJ.TogaA. W.DinovI. D.WorthmanC. M.SowellE. R. (2011). Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cerebral Cortex, 21(3), 636–646. https://doi.org/10.1093/cercor/bhq137
6.
CaldwellB. M.AndersonN. E.HarenskiK. A.SitneyM. H.CaldwellM. F.Van RybroekG. J.KiehlK. A. (2019). The structural brain correlates of callous-unemotional traits in incarcerated male adolescents. NeuroImage: Clinical, 22, Article 101703. https://doi.org/10.1016/j.nicl.2019.101703
7.
CardinaleE. M.O’ConnellK.RobertsonE. L.MeenaL. B.BreedenA. L.LozierL. M.VanMeterJ. W.MarshA. A. (2019). Callous and uncaring traits are associated with reductions in amygdala volume among youths with varying levels of conduct problems. Psychological Medicine, 49(9), 1449–1458. https://doi.org/10.1017/S0033291718001927
8.
ChoyO.RaineA.PortnoyJ.Rudo-HuttA.GaoY.SoyferL. (2015). The mediating role of heart rate on the social adversity-antisocial behavior relationship: A social neurocriminology perspective. Journal of Research in Crime and Delinquency, 52(3), 303–341. https://doi.org/10.1177/0022427814565905
9.
De BritoS. A.MechelliA.WilkeM.LaurensK. R.JonesA. P.BarkerG. J.HodginsS.VidingE. (2009). Size matters: Increased grey matter in boys with conduct problems and callous unemotional traits. Brain, 132(4), 843–852. https://doi.org/10.1093/brain/awp011
10.
FairchildG.HaganC. C.WalshN. D.PassamontiL.CalderA. J.GoodyerI. M. (2013). Brain structure abnormalities in adolescent girls with conduct disorder. Journal of Child Psychology and Psychiatry and Allied Disciplines, 54(1), 86–95. https://doi.org/10.1111/j.1469-7610.2012.02617.x
11.
FairchildG.PassamontiL.HurfordG.HaganC. C.Von Dem HagenE. A. H.Van GoozenS. H. M.GoodyerI. M.CalderA. J. (2011). Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. American Journal of Psychiatry, 168(6), 624–633. https://doi.org/10.1176/appi.ajp.2010.10081184
12.
FairchildG.Van GoozenS. H. M.CalderA. J.GoodyerI. M. (2013). Research review: Evaluating and reformulating the developmental taxonomic theory of antisocial behaviour. Journal of Child Psychology and Psychiatry and Allied Disciplines, 54(9), 924–940. https://doi.org/10.1111/jcpp.12102
FischlB.SalatD. H.BusaE.AlbertM.DieterichM.HaselgroveC.Van Der KouweA.KillianyR.KennedyD.KlavenessS.MontilloA.MakrisN.RosenB.DaleA. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355. https://doi.org/10.1016/S0896-6273(02)00569-X
15.
FishA. M.NadigA.SeidlitzJ.ReardonP. K.MankiwC.McDermottC. L.BlumenthalJ. D.ClasenL. S.LalondeF.LerchJ. P.ChakravartyM. M.ShinoharaR. T.RaznahanA. (2020). Sex-biased trajectories of amygdalo-hippocampal morphology change over human development. Neuroimage, 201, Article 116122. https://doi.org/10.1016/j.neuroimage.2019.116122
16.
FrickP. J.CornellA. H.BodinS. D.DaneH. E.BarryC. T.LoneyB. R. (2003). Callous-unemotional traits and developmental pathways to severe conduct problems. Developmental Psychology, 39(2), 246–260. https://doi.org/10.1037/0012-1649.39.2.246
17.
FrickP. J.HareR. (2001). Antisocial process screening device: APSD. Multi-Health Systems.
18.
FrickP. J.RayJ. V.ThorntonL. C.KahnR. E. (2014). Annual research review: A developmental psychopathology approach to understanding callous-unemotional traits in children and adolescents with serious conduct problems. Journal of Child Psychology and Psychiatry and Allied Disciplines, 55(6), 532–548. https://doi.org/10.1111/jcpp.12152
19.
FrickP. J.WhiteS. F. (2008). Research review: The importance of callous-unemotional traits for developmental models of aggressive and antisocial behavior. Journal of Child Psychology and Psychiatry and Allied Disciplines, 49(4), 359–375. https://doi.org/10.1111/j.1469-7610.2007.01862.x
20.
GieddJ. N.ClasenL. S.LenrootR.GreensteinD.WallaceG. L.OrdazS.MolloyE. A.BlumenthalJ. D.TossellJ. W.StayerC.Samango-SprouseC. A.ShenD.DavatzikosC.MerkeD.ChrousosG. P. (2006). Puberty-related influences on brain development. Molecular and Cellular Endocrinology, 254–255, 154–162. https://doi.org/10.1016/j.mce.2006.04.016
21.
GlennA. L. (2019). Early life predictors of callous-unemotional and psychopathic traits. Infant Mental Health Journal, 40(1), 39–53. https://doi.org/10.1002/imhj.21757
22.
GoddingsA. L.MillsK. L.ClasenL. S.GieddJ. N.VinerR. M.BlakemoreS. J. (2014). The influence of puberty on subcortical brain development. NeuroImage, 88, 242–251. https://doi.org/10.1016/j.neuroimage.2013.09.073
KahnR. E.FrickP. J.YoungstromE. A.YoungstromJ. K.FeenyN. C.FindlingR. L. (2013). Distinguishing primary and secondary variants of callous-unemotional traits among adolescents in a clinic-referred sample. Psychological Assessment, 25(3), 966–978. https://doi.org/10.1037/a0032880
25.
LiuJ.RichmondT. S.RaineA.CheneyR.BrodkinE. S.GurR. C.GurR. E. (2013). The healthy brains and behavior study: Objectives, design, recruitment, and population coverage. International Journal of Methods in Psychiatric Research, 22(3), 204–216. https://doi.org/10.1002/mpr.1394
26.
Martin-KeyN.BrownT.FairchildG. (2017). Empathic accuracy in male adolescents with conduct disorder and higher versus lower levels of callous-unemotional traits. Journal of Abnormal Child Psychology, 45, 1385–1397. https://doi.org/10.1007/s10802-016-0243-8
27.
McDonough-CaplanH. M.BeauchaineT. P. (2018). Conduct disorder: A neurodevelopmental perspective. In MartelM. M. (Ed.), Developmental pathways to disruptive, impulse-control and conduct disorders, (pp. 53–89). https://doi.org/10.1016/B978-0-12-811323-3.00003-1
28.
MoffittT. E. (1993). Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy. Psychological Review, 100(4), 674–701. https://doi.org/10.1037/0033-295X.100.4.674
29.
National Institute of Mental Health. (2011). Sex differences in brain, behavior, mental health and mental disorders.
30.
National Institutes of Health. (2015). Moving into the future with new dimensions and strategies: A vision for 2020 for women’s health research.
31.
NeufangS.SpechtK.HausmannM.GüntürkünO.Herpertz-DahlmannB.FinkG. R.KonradK. (2009). Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex, 19(2), 464–473. https://doi.org/10.1093/cercor/bhn100
32.
PiacentiniJ. C.CohenP.CohenJ. (1992). Combining discrepant diagnostic information from multiple sources: Are complex algorithms better than simple ones?Journal of Abnormal Child Psychology, 20, 51–63. https://doi.org/10.1007/BF00927116
RaineA.MeloyJ. R.BihrleS.StoddardJ.LaCasseL.BuchsbaumM. S. (1998). Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behavioral Sciences and the Law, 16(3), 319–332. https://doi.org/10.1002/(SICI)1099-0798(199822)16:3<319::AID-BSL311>3.0.CO;2-G
38.
RaschleN. M.MenksW. M.FehlbaumL. V.SteppanM.SmaragdiA.Gonzalez-MadrugaK.RogersJ.ClantonR.KohlsG.MartinelliA.BernhardA.KonradK.Herpertz-DahlmannB.FreitagC. M.FairchildG.De BritoS. A.StadlerC. (2018). Callous-unemotional traits and brain structure: Sex-specific effects in anterior insula of typically-developing youths. NeuroImage: Clinical, 17, 856–864. https://doi.org/10.1016/j.nicl.2017.12.015
39.
RichmondT. S.CheneyR.SoyferL.KimmelR.RaineA. (2013). Recruitment of community-residing youth into studies on aggression. Journal of Community Psychology, 41(4), 425–434. https://doi.org/10.1002/jcop.21546
40.
RogersJ. C.De BritoS. A. (2016). Cortical and subcortical gray matter volume in youths with conduct problems a meta-analysis. JAMA Psychiatry, 73(1), 64–72. https://doi.org/10.1001/jamapsychiatry.2015.2423
41.
SatterthwaiteT. D.ShinoharaR. T.WolfD. H.HopsonR. D.ElliottM. A.VandekarS. N.RuparelK.CalkinsM. E.RoalfD. R.GennatasE. D.JacksonC.ErusG.PrabhakaranK.DavatzikosC.DetreJ. A.HakonarsonH.GurR. C.GurR. E. (2014). Impact of puberty on the evolution of cerebral perfusion during adolescence. Proceedings of the National Academy of Sciences of the United States of America, 111(23), 8643–8648. https://doi.org/10.1073/pnas.1400178111
42.
SchwenckC.CiaramidaroA.SelivanovaM.TournayJ.FreitagC. M.SiniatchkinM. (2017). Neural correlates of affective empathy and reinforcement learning in boys with conduct problems: fMRI evidence from a gambling task. Behavioural Brain Research, 320, 75–84. https://doi.org/10.1016/j.bbr.2016.11.037
43.
SchwenckC.MergenthalerJ.KellerK.ZechJ.SalehiS.TaurinesR.RomanosM.SchecklmannM.SchneiderW.WarnkeA.FreitagC. M. (2012). Empathy in children with autism and conduct disorder: Group-specific profiles and developmental aspects. Journal of Child Psychology and Psychiatry and Allied Disciplines, 53(6), 651–659. https://doi.org/10.1111/j.1469-7610.2011.02499.x
44.
SebastianC. L.De BritoS. A.McCroryE. J.HydeZ. H.LockwoodP. L.CecilC. A. M.VidingE. (2016). Grey matter volumes in children with conduct problems and varying levels of callous-unemotional traits. Journal of Abnormal Child Psychology, 44, 639–649. https://doi.org/10.1007/s10802-015-0073-0
45.
SebastianC. L.McCroryE. J.DaddsM. R.CecilC. A. M.LockwoodP. L.HydeZ. H.De BritoS. A.VidingE. (2014). Neural responses to fearful eyes in children with conduct problems and varying levels of callous-unemotional traits. Psychological Medicine, 44(1), 99–109. https://doi.org/10.1017/S0033291713000482
46.
SiepN.TonnaerF.van de VenV.ArntzA.RaineA.CimaM. (2019). Anger provocation increases limbic and decreases medial prefrontal cortex connectivity with the left amygdala in reactive aggressive violent offenders. Brain Imaging and Behavior, 13, 1311–1323. https://doi.org/10.1007/s11682-018-9945-6
47.
SterzerP.StadlerC.PoustkaF.KleinschmidtA. (2007). A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. NeuroImage, 37(1), 335–342. https://doi.org/10.1016/j.neuroimage.2007.04.043
48.
SzabóE.KocselN.ÉdesA.PapD.GalambosA.ZsombókT.SzabóÁ.KozákL. R.BagdyG.JuhászG.KökönyeiG. (2017). Callous-unemotional traits and neural responses to emotional faces in a community sample of young adults. Personality and Individual Differences, 111, 312–317. https://doi.org/10.1016/j.paid.2017.02.026
TottenhamN.GalvánA. (2016). Stress and the adolescent brain: Amygdala-prefrontal cortex circuitry and ventral striatum as developmental targets. Neuroscience and Biobehavioral Reviews, 70, 217–227. https://doi.org/10.1016/j.neubiorev.2016.07.030
51.
TranelD.DamasioH.DenburgN. L.BecharaA. (2005). Does gender play a role in functional asymmetry of ventromedial prefrontal cortex?Brain, 128(12), 2872–2881. https://doi.org/10.1093/brain/awh643
52.
UematsuA.MatsuiM.TanakaC.TakahashiT.NoguchiK.SuzukiM.NishijoH. (2012). Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLOS ONE, 7(10), Article e46970. https://doi.org/10.1371/journal.pone.0046970
53.
VidingE.SebastianC. L.DaddsM. R.LockwoodP. L.CecilC. A. M.De BritoS. A.McCroryE. J. (2012). Amygdala response to preattentive masked fear in children with conduct problems: The role of callous-unemotional traits. American Journal of Psychiatry, 169(10), 1109–1116. https://doi.org/10.1176/appi.ajp.2012.12020191
54.
VisserT. A. W.OhanJ. L.WhittleS.YücelM.SimmonsJ. G.AllenN. B. (2014). Sex differences in structural brain asymmetry predict overt aggression in early adolescents. Social Cognitive and Affective Neuroscience, 9(4), 553–560. https://doi.org/10.1093/scan/nst013
55.
WakschlagL. S.PerlmanS. B.BlairR. J.LeibenluftE.Briggs-GowanM. J.PineD. S. (2018). The neurodevelopmental basis of early childhood disruptive behavior: Irritable and callous phenotypes as exemplars. American Journal of Psychiatry, 175(2), 114–130. https://doi.org/10.1176/appi.ajp.2017.17010045
56.
WallaceG. L.WhiteS. F.RobustelliB.SinclairS.HwangS.MartinA.BlairR. J. R. (2014). Cortical and subcortical abnormalities in youths with conduct disorder and elevated callous-unemotional traits. Journal of the American Academy of Child and Adolescent Psychiatry, 53(4), 456–465. https://doi.org/10.1016/j.jaac.2013.12.008
57.
WallerR.GardnerF.HydeL. W.ShawD. S.DishionT. J.WilsonM. N. (2012). Do harsh and positive parenting predict parent reports of deceitful-callous behavior in early childhood?Journal of Child Psychology and Psychiatry and Allied Disciplines, 53(9), 946–953. https://doi.org/10.1111/j.1469-7610.2012.02550.x
58.
WallerR.HydeL. W. (2018). Callous-unemotional behaviors in early childhood: The development of empathy and prosociality gone awry. Current Opinion in Psychology, 20, 11–16. https://doi.org/10.1016/j.copsyc.2017.07.037
59.
WallerR.WagnerN. J.BarsteadM. G.SubarA.PetersenJ. L.HydeJ. S.HydeL. W. (2019). A meta-analysis of the associations between callous-unemotional traits and empathy, prosociality, and guilt. Clinical Psychology Review, 75, Article 101809.
60.
WhiteS. F.CruiseK. R.FrickP. J. (2009). Differential correlates to self-report and parent-report of callous-unemotional traits in a sample of juvenile sexual offenders. Behavioral Sciences and the Law, 27(6), 910–928. https://doi.org/10.1002/bsl.911
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