Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-17T20:14:02.260Z Has data issue: false hasContentIssue false

Neural responses to fearful eyes in children with conduct problems and varying levels of callous–unemotional traits

Published online by Cambridge University Press:  19 March 2013

C. L. Sebastian*
Affiliation:
Division of Psychology and Language Sciences, University College London, UK Department of Psychology, Royal Holloway, University of London, Egham, Surrey, UK
E. J. McCrory
Affiliation:
Division of Psychology and Language Sciences, University College London, UK
M. R. Dadds
Affiliation:
School of Psychology, University of New South Wales, Sydney, NSW, Australia
C. A. M. Cecil
Affiliation:
Division of Psychology and Language Sciences, University College London, UK
P. L. Lockwood
Affiliation:
Division of Psychology and Language Sciences, University College London, UK
Z. H. Hyde
Affiliation:
Division of Psychology and Language Sciences, University College London, UK
S. A. De Brito
Affiliation:
School of Psychology, University of Birmingham, Edgbaston, Birmingham, UK
E. Viding*
Affiliation:
Division of Psychology and Language Sciences, University College London, UK
*
*Author for correspondence: E. Viding, Division of Psychology and Language Sciences, University College London, 26 Bedford Way, London WC1H 0AP, UK. (Email: e.viding@ucl.ac.uk) [E. Viding] (Email: catherine.sebastian@rhul.ac.uk) [C. L. Sebastian]
*Author for correspondence: E. Viding, Division of Psychology and Language Sciences, University College London, 26 Bedford Way, London WC1H 0AP, UK. (Email: e.viding@ucl.ac.uk) [E. Viding] (Email: catherine.sebastian@rhul.ac.uk) [C. L. Sebastian]

Abstract

Background

Children with conduct problems (CP) are a heterogeneous group. Those with high levels of callous–unemotional traits (CP/HCU) appear emotionally under-reactive at behavioural and neural levels whereas those with low levels of CU traits (CP/LCU) appear emotionally over-reactive, compared with typically developing (TD) controls. Investigating the degree to which these patterns of emotional reactivity are malleable may have important translational implications. Instructing participants with CP/HCU to focus on the eyes of fearful faces (i.e. the most salient feature) can ameliorate their fear-recognition deficits, but it is unknown whether this is mediated by amygdala response. It is also unknown whether focusing on fearful eyes is associated with increased amygdala reactivity in CP/LCU.

Method

Functional magnetic resonance imaging (fMRI) was used to measure neural responses to fearful and calm faces in children with CP/HCU, CP/LCU and TD controls (n = 17 per group). On half of trials participants looked for a blue dot anywhere within target faces; on the other half, participants were directed to focus on the eye region.

Results

Reaction time (RT) data showed that CP/LCU were selectively slowed in the fear/eyes condition. For the same condition, CP/LCU also showed increased amygdala and subgenual anterior cingulate cortex (sgACC)/orbitofrontal cortex (OFC) responses compared with TD controls. RT and amygdala response to fear/eyes were correlated in CP/LCU only. No effects of focusing on the eye region were observed in CP/HCU.

Conclusions

These data extend the evidence base suggesting that CU traits index meaningful heterogeneity in conduct problems. Focusing on regulating reactive emotional responses may be a fruitful strategy for children with CP/LCU.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolphs, R, Gosselin, F, Buchanan, TW, Tranel, D, Schyns, P, Damasio, AR (2005). A mechanism for impaired fear recognition after amygdala damage. Nature 433, 6872.Google Scholar
Babor, TF, Higgins-Biddle, JC, Saunders, JB, Monteiro, MG (2001). The Alcohol Use Disorders Identification Test: Guidelines for Use in Primary Care, 2nd edn. Department of Mental Health and Substance Dependence, World Health Organization: Geneva.Google Scholar
Baskin-Sommers, AR, Curtin, JJ, Larson, CL, Stout, D, Kiehl, KA, Newman, JP (2012). Characterizing the anomalous cognition-emotion interactions in externalizing. Biological Psychology 91, 4858.Google Scholar
Berman, AH, Bergman, H, Palmstierna, T, Schlyter, F (2005). Evaluation of the Drug Use Disorders Identification Test (DUDIT) in criminal justice and detoxification settings and in a Swedish population sample. European Addiction Research 11, 2231.CrossRefGoogle Scholar
Blair, RJR, Budhani, S, College, E, Scott, S (2005). Deafness to fear in boys with psychopathic tendencies. Journal of Child Psychology and Psychiatry 46, 327336.Google Scholar
Blair, RJR, Colledge, E, Murray, L, Mitchell, DVG (2001). A selective impairment in the processing of sad and fearful expressions in children with psychopathic tendencies. Journal of Abnormal Child Psychology 29, 491498.Google Scholar
Dadds, MR, El Masry, Y, Wimalaweera, S, Guastella, AJ (2008). Reduced eye gaze explains ‘fear blindness’ in childhood psychopathic traits. Journal of the American Academy of Child and Adolescent Psychiatry 47, 455463.Google Scholar
Dadds, MR, Perry, Y, Hawes, DJ, Merz, S, Riddell, AC, Haines, DJ, Solak, E, Abeygunawardane, AI (2006). Attention to the eyes and fear-recognition deficits in child psychopathy. British Journal of Psychiatry 189, 280281.Google Scholar
Drevets, WC, Savitz, J, Trimble, M (2008). The subgenual anterior cingulate cortex in mood disorders. CNS Spectrums 13, 663681.Google Scholar
Eisenberg, N, Spinrad, TL, Eggum, ND (2010). Emotion-related self-regulation and its relation to children's maladjustment. Annual Review of Clinical Psychology 6, 495525.Google Scholar
Frick, PJ, Cornell, AH, Bodin, SD, Dane, HE, Barry, CT, Loney, BR (2003 a). Callous-unemotional traits and developmental pathways to severe conduct problems. Developmental Psychology 39, 246260.Google Scholar
Frick, PJ, Kimonis, ER, Dandreaux, DM, Farrell, JM (2003 b). The 4-year stability of psychopathic traits in nonreferred youth. Behavioral Sciences and the Law 21, 713736.Google Scholar
Frick, PJ, Morris, AS (2004). Temperament and developmental pathways to conduct problems. Journal of Clinical Child and Adolescent Psychology 33, 5468.CrossRefGoogle ScholarPubMed
Frick, PJ, Viding, E (2009). Antisocial behavior from a developmental psychopathology perspective. Development and Psychopathology 21, 11111131.Google Scholar
Gadow, KD, Sprafkin, J (2009). The Symptom Inventories: An Annotated Bibliography. Checkmate Plus: Stony Brook, New York.Google Scholar
Gamer, M, Buchel, C (2009). Amygdala activation predicts gaze toward fearful eyes. Journal of Neuroscience 29, 91239126.CrossRefGoogle ScholarPubMed
Herpertz, SC, Huebner, T, Marx, I, Vloet, TD, Fink, GR, Stoecker, T, Shah, NJ, Konrad, K, Herpertz-Dahlmann, B (2008). Emotional processing in male adolescents with childhood-onset conduct disorder. Journal of Child Psychology and Psychiatry 49, 781791.Google Scholar
Jones, AP, Laurens, KR, Herba, CM, Barker, GJ, Viding, E (2009). Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. American Journal of Psychiatry 166, 95102.CrossRefGoogle ScholarPubMed
Lieberman, MD, Cunningham, WA (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423428.CrossRefGoogle ScholarPubMed
Loney, BR, Frick, PJ, Clements, CB, Ellis, ML, Kerlin, K (2003). Callous-unemotional traits, impulsivity, and emotional processing in adolescents with antisocial behavior problems. Journal of Clinical Child and Adolescent Psychology 32, 6680.Google Scholar
Marsh, AA, Finger, EC, Mitchell, DGV, Reid, ME, Sims, C, Kosson, DS, Towbin, KE, Leibenluft, E, Pine, DS, Blair, RJR (2008). Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. American Journal of Psychiatry 165, 712720.Google Scholar
Marsh, AA, Finger, EC, Schechter, JC, Jurkowitz, IT, Reid, ME, Blair, RJ (2011). Adolescents with psychopathic traits report reductions in physiological responses to fear. Journal of Child Psychology and Psychiatry 52, 834841.Google Scholar
Moul, C, Killcross, S, Dadds, MR (2012). A model of differential amygdala activation in psychopathy. Psychological Review 119, 789806.Google Scholar
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242249.CrossRefGoogle ScholarPubMed
Passamonti, L, Fairchild, G, Goodyer, IM, Hurford, G, Hagan, CC, Rowe, JB, Calder, AJ (2010). Neural abnormalities in early-onset and adolescence-onset conduct disorder. Archives of General Psychiatry 67, 729738.CrossRefGoogle ScholarPubMed
Pessoa, L (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience 9, 148158.Google Scholar
Phillips, ML, Medford, N, Young, AW, Williams, L, Williams, SC, Bullmore, ET, Gray, JA, Brammer, MJ (2001). Time courses of left and right amygdalar responses to fearful facial expressions. Human Brain Mapping 12, 193202.Google Scholar
Romeo, R, Knapp, M, Scott, S (2006). Economic cost of severe antisocial behaviour in children – and who pays it. British Journal of Psychiatry 188, 547553.Google Scholar
Sebastian, CL, McCrory, EJ, Cecil, CA, Lockwood, PL, De Brito, SA, Fontaine, NM, Viding, E (2012). Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits. Archives of General Psychiatry 69, 814822.Google Scholar
Sharp, C, van Goozen, S, Goodyer, I (2006). Children's subjective emotional reactivity to affective pictures: gender differences and their antisocial correlates in an unselected sample of 7–11-year-olds. Journal of Child Psychology and Psychiatry 47, 143150.Google Scholar
Sterzer, P, Stadler, C, Krebs, A, Kleinschmidt, A, Poustka, F (2005). Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biological Psychiatry 57, 715.Google Scholar
Tottenham, N, Tanaka, JW, Leon, AC, McCarry, T, Nurse, M, Hare, TA, Marcus, DJ, Westerlund, A, Casey, BJ, Nelson, C (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 242249.Google Scholar
Viding, E, Sebastian, CL, Dadds, MR, Lockwood, PL, Cecil, CAM, De Brito, SA, McCrory, EJ (2012). Amygdala response to pre-attentive masked fear is associated with callous-unemotional traits in children with conduct problems. American Journal of Psychiatry 169, 11091116.Google Scholar
Weiskopf, N, Hutton, C, Josephs, O, Deichmann, R (2006). Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a whole-brain analysis at 3 T and 1.5 T. NeuroImage 33, 493504.Google Scholar
Weschler, D (1999). Wechsler Abbreviated Scale of Intelligence (WASI). Harcourt Assessment: San Antonio, TX.Google Scholar
White, SF, Williams, WC, Brislin, SJ, Sinclair, S, Blair, KS, Fowler, KA, Pine, DS, Pope, K, Blair, RJ (2012). Reduced activity within the dorsal endogenous orienting of attention network to fearful expressions in youth with disruptive behavior disorders and psychopathic traits. Development and Psychopathology 24, 11051116.Google Scholar
Zikopoulos, B, Barbas, HJ (2012). Pathways for emotions and attention converge on the thalamic reticular nucleus in primates. Journal of Neuroscience 32, 53385350.Google Scholar
Supplementary material: File

Sebastian supplementary material

Sebastian supplementary material

Download Sebastian supplementary material(File)
File 43 KB