Display options
Cite
Böttinger BW, Baumeister S, Millenet S, et al. Orbitofrontal control of conduct problems? Evidence from healthy adolescents processing negative facial affect. Eur Child Adolesc Psychiatry. 2021;doi: 10.1007/s00787-021-01770-1.
Böttinger, B. W., Baumeister, S., Millenet, S., Barker, G. J., Bokde, A. L. W., Büchel, C., Quinlan, E. B., Desrivières, S., Flor, H., Grigis, A., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Martinot, J. L., Martinot, M. P., Artiges, E., Orfanos, D. P., Paus, T., Poustka, L., Fröhner, J. H., Smolka, M. N., Walter, H., Whelan, R., Schumann, G., Banaschewski, T., Brandeis, D., Nees, F. (2021). Orbitofrontal control of conduct problems? Evidence from healthy adolescents processing negative facial affect. European child & adolescent psychiatry, . https://doi.org/10.1007/s00787-021-01770-1
Böttinger, Boris William, et al. "Orbitofrontal control of conduct problems? Evidence from healthy adolescents processing negative facial affect." European child & adolescent psychiatry vol. (2021). doi: https://doi.org/10.1007/s00787-021-01770-1
Böttinger BW, Baumeister S, Millenet S, Barker GJ, Bokde ALW, Büchel C, Quinlan EB, Desrivières S, Flor H, Grigis A, Garavan H, Gowland P, Heinz A, Ittermann B, Martinot JL, Martinot MP, Artiges E, Orfanos DP, Paus T, Poustka L, Fröhner JH, Smolka MN, Walter H, Whelan R, Schumann G, Banaschewski T, Brandeis D, Nees F. Orbitofrontal control of conduct problems? Evidence from healthy adolescents processing negative facial affect. Eur Child Adolesc Psychiatry. 2021 Apr 16; doi: 10.1007/s00787-021-01770-1. Epub 2021 Apr 16. PMID: 33861383.
Copy Download .nbib Format: NLM
Share it on

Eur Child Adolesc Psychiatry. 2021 Apr 16; doi: 10.1007/s00787-021-01770-1. Epub 2021 Apr 16.

Orbitofrontal control of conduct problems? Evidence from healthy adolescents processing negative facial affect.

European child & adolescent psychiatry

Boris William Böttinger, Sarah Baumeister, Sabina Millenet, Gareth J Barker, Arun L W Bokde, Christian Büchel, Erin Burke Quinlan, Sylvane Desrivières, Herta Flor, Antoine Grigis, Hugh Garavan, Penny Gowland, Andreas Heinz, Bernd Ittermann, Jean-Luc Martinot, Marie-Laure Paillère Martinot, Eric Artiges, Dimitri Papadopoulos Orfanos, Tomáš Paus, Luise Poustka, Juliane H Fröhner, Michael N Smolka, Henrik Walter, Robert Whelan, Gunter Schumann, Tobias Banaschewski, Daniel Brandeis, Frauke Nees,

Affiliations

  1. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany. [email protected].
  2. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
  3. Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
  4. Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
  5. University Medical Centre Hamburg-Eppendorf, House W34, 3.OG, Martinistr. 52, 20246, Hamburg, Germany.
  6. Medical Research Council, Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
  7. Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany.
  8. Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
  9. NeuroSpin, CEA, Université Paris-Saclay, 91191, Gif-sur-Yvette, France.
  10. Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, 05405, USA.
  11. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK.
  12. Department of Psychiatry and Psychotherapy, Charité, Universitätsmedizin Berlin, Campus Charité Mitte, Charitéplatz 1, Berlin, Germany.
  13. Freie Universität Berlin, Berlin, Germany.
  14. Humboldt-Universität Zu Berlin, Berlin, Germany.
  15. Berlin Institute of Health, Berlin, Germany.
  16. Physikalisch-Technische Bundesanstalt (PTB), Abbestr. 2-12, Berlin, Germany.
  17. Physikalisch-Technische Bundesanstalt (PTB), Braunschweig, Germany.
  18. Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging and Psychiatry", University Paris Sud, University Paris Descartes, Sorbonne Paris Cité, Paris, France.
  19. Maison de Solenn, Paris, France.
  20. Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging and Psychiatry", University Paris Sud, University Paris Descartes; Sorbonne Université, Paris, France.
  21. AP-HP, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
  22. Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging and Psychiatry", University Paris Sud, University Paris Descartes, Sorbonne Paris Cité, Orsay, France.
  23. Psychiatry Department 91G16, Orsay Hospital, Orsay, France.
  24. Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital and Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, M6A 2E1, Canada.
  25. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany.
  26. Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
  27. School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
  28. Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland.
  29. Zurich Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland.
  30. Neuroscience Centre Zurich, University and ETH Zurich, Zurich, Switzerland.

PMID: 33861383 DOI: 10.1007/s00787-021-01770-1

Abstract

Conduct problems (CP) in patients with disruptive behavior disorders have been linked to impaired prefrontal processing of negative facial affect compared to controls. However, it is unknown whether associations with prefrontal activity during affective face processing hold along the CP dimension in a healthy population sample, and how subcortical processing is affected. We measured functional brain responses during negative affective face processing in 1444 healthy adolescents [M = 14.39 years (SD = 0.40), 51.5% female] from the European IMAGEN multicenter study. To determine the effects of CP, we applied a two-step approach: (a) testing matched subgroups of low versus high CP, extending into the clinical range [N = 182 per group, M = 14.44 years, (SD = 0.41), 47.3% female] using analysis of variance, and (b) considering (non)linear effects along the CP dimension in the full sample and in the high CP group using multiple regression. We observed no significant cortical or subcortical effect of CP group on brain responses to negative facial affect. In the full sample, regression analyses revealed a significant linear increase of left orbitofrontal cortex (OFC) activity with increasing CP up to the clinical range. In the high CP group, a significant inverted u-shaped effect indicated that left OFC responses decreased again in individuals with high CP. Left OFC activity during negative affective processing which is increasing with CP and decreasing in the highest CP range may reflect on the importance of frontal control mechanisms that counteract the consequences of severe CP by facilitating higher social engagement and better evaluation of social content in adolescents.

Keywords: Adolescence; Affective processing; Conduct problems; FMRI; Orbitofrontal cortex; Subclinical

References

  1. Odgers CL, Caspi A, Broadbent JM, Dickson N, Hancox RJ, Harrington H et al (2007) Prediction of differential adult health burden by conduct problem subtypes in males. Arch Gen Psychiatry 64(4):476–484 - PubMed
  2. Loeber R, Burke JD, Lahey BB, Winters A, Zera M (2000) Oppositional defiant and conduct disorder: a review of the past 10 years, part I. J Am Acad Child Adolesc Psychiatry 39(12):1468–1484 - PubMed
  3. Viding E, Sebastian CL, Dadds MR, Lockwood PL, Cecil CA, De Brito SA et al (2012) Amygdala response to preattentive masked fear in children with conduct problems: the role of callous-unemotional traits. Am J Psychiatry 169(10):1109–1116 - PubMed
  4. Fairchild G, van Goozen SH, Calder AJ, Goodyer IM (2013) Research review: evaluating and reformulating the developmental taxonomic theory of antisocial behaviour. J Child Psychol Psychiatry 54(9):924–940 - PubMed
  5. Blair RJR, Veroude K, Buitelaar JK (2018) Neuro-cognitive system dysfunction and symptom sets: a review of fMRI studies in youth with conduct problems. Neurosci Biobehav Rev 91:69–90 - PubMed
  6. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48(2):175–187 - PubMed
  7. Lindquist KA, Satpute AB, Wager TD, Weber J, Barrett LF (2016) The brain basis of positive and negative affect: evidence from a meta-analysis of the human neuroimaging literature. Cerebral Cortex (New York, NY: 1991) 26(5):1910–1922 - PubMed
  8. Müller VI, Höhner Y, Eickhoff SB (2018) Influence of task instructions and stimuli on the neural network of face processing: an ALE meta-analysis. Cortex 103:240–255 - PubMed
  9. García-García I, Kube J, Gaebler M, Horstmann A, Villringer A, Neumann J (2016) Neural processing of negative emotional stimuli and the influence of age, sex and task-related characteristics. Neurosci Biobehav Rev 68:773–793 - PubMed
  10. Hyde LW, Byrd AL, Votruba-Drzal E, Hariri AR, Manuck SB (2014) Amygdala reactivity and negative emotionality: divergent correlates of antisocial personality and psychopathy traits in a community sample. J Abnorm Psychol 123(1):214–224 - PubMed
  11. Hyde LW, Shaw DS, Murray L, Gard A, Hariri AR, Forbes EE (2016) Dissecting the role of amygdala reactivity in antisocial behavior in a sample of young, low-income, urban men. Clin Psychol Sci 4(3):527–544 - PubMed
  12. Davidson RJ, Putnam KM, Larson CL (2000) Dysfunction in the neural circuitry of emotion regulation–a possible prelude to violence. Science (New York, NY) 289(5479):591–594 - PubMed
  13. Davidson RJ, Jackson DC, Kalin NH (2000) Emotion, plasticity, context, and regulation: perspectives from affective neuroscience. Psychol Bull 126(6):890 - PubMed
  14. Yang M, Tsai SJ, Li CR (2020) Concurrent amygdalar and ventromedial prefrontal cortical responses during emotion processing: a meta-analysis of the effects of valence of emotion and passive exposure versus active regulation. Brain Struct Funct 225(1):345–363 - PubMed
  15. Riedel MC, Yanes JA, Ray KL, Eickhoff SB, Fox PT, Sutherland MT et al (2018) Dissociable meta-analytic brain networks contribute to coordinated emotional processing. Hum Brain Mapp 39(6):2514–2531 - PubMed
  16. Viding E, McCrory EJ (2018) Understanding the development of psychopathy: progress and challenges. Psychol Med 48(4):566–577 - PubMed
  17. Yang Y, Raine A (2009) Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Res 174(2):81–88 - PubMed
  18. Rubia K (2011) “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiat 69(12):e69-87 - PubMed
  19. Sterzer P, Stadler C, Krebs A, Kleinschmidt A, Poustka F (2005) Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biol Psychiat 57(1):7–15 - PubMed
  20. Passamonti L, Fairchild G, Goodyer IM, Hurford G, Hagan CC, Rowe JB et al (2010) Neural abnormalities in early-onset and adolescence-onset conduct disorder. Arch Gen Psychiatry 67(7):729–738 - PubMed
  21. Fairchild G, Hagan CC, Passamonti L, Walsh ND, Goodyer IM, Calder AJ (2014) Atypical neural responses during face processing in female adolescents with conduct disorder. J Am Acad Child Adolesc Psychiatry 53(6):677-687.e675 - PubMed
  22. Decety J, Skelly L, Yoder KJ, Kiehl KA (2014) Neural processing of dynamic emotional facial expressions in psychopaths. Soc Neurosci 9(1):36–49 - PubMed
  23. Herpertz SC, Huebner T, Marx I, Vloet TD, Fink GR, Stoecker T et al (2008) Emotional processing in male adolescents with childhood-onset conduct disorder. J Child Psychol Psychiatry 49(7):781–791 - PubMed
  24. 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. Am J Psychiatry 166(1):95–102 - PubMed
  25. Baker RH, Clanton RL, Rogers JC, De Brito SA (2015) Neuroimaging findings in disruptive behavior disorders. CNS Spectr 20(4):369–381 - PubMed
  26. Sebastian C, McCrory E, Dadds M, Cecil C, Lockwood P, Hyde Z et al (2014) Neural responses to fearful eyes in children with conduct problems and varying levels of callous–unemotional traits. Psychol Med 44(1):99–109 - PubMed
  27. Hwang S, Nolan ZT, White SF, Williams WC, Sinclair S, Blair RJ (2016) Dual neurocircuitry dysfunctions in disruptive behavior disorders: emotional responding and response inhibition. Psychol Med 46(7):1485–1496 - PubMed
  28. Spechler PA, Chaarani B, Orr C, Mackey S, Higgins ST, Banaschewski T, et al. (2019) Neuroimaging Evidence for Right Orbitofrontal Cortex Differences in Adolescents With Emotional and Behavioral Dysregulation. J Am Acad Child Adolescent Psychiatry - PubMed
  29. De Brito SA, Mechelli A, Wilke M, Laurens KR, Jones AP, Barker GJ et al (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain: J Neurol 132(Pt 4):843–852 - PubMed
  30. Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Buchel C et al (2010) The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry 15(12):1128–1139 - PubMed
  31. Goodman R (1997) The strengths and difficulties questionnaire: a research note. J Child Psychol Psychiatry 38(5):581–586 - PubMed
  32. Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 17(2):117–133 - PubMed
  33. Petermann FP (2011) U. (Hrsg.) Wechsler Intelligence Scale for Children—Fourth Edition. Manual 1: Grundlagen, Testauswertung und Interpretation. Übersetzung und Adaptation der WISC-IV von David Wechsler. Frankfurt: Pearson - PubMed
  34. Grosbras MH, Paus T (2006) Brain networks involved in viewing angry hands or faces. Cerebral Cortex (New York, NY: 1991). 16(8):1087–1096 - PubMed
  35. Davids M, Zöllner FG, Ruttorf M, Nees F, Flor H, Schumann G et al (2014) Fully-automated quality assurance in multi-center studies using MRI phantom measurements. Magn Reson Imaging 32(6):771–780 - PubMed
  36. Allen EA, Erhardt EB, Calhoun VD (2012) Data visualization in the neurosciences: overcoming the curse of dimensionality. Neuron 74(4):603–608 - PubMed
  37. Zandbelt B (2017) Slice Display. figshare - PubMed
  38. Truedsson E, Fawcett C, Wesevich V, Gredeback G, Wahlstedt C (2019) The role of callous-unemotional traits on adolescent positive and negative emotional reactivity: a longitudinal community-based study. Front Psychol 10:573 - PubMed
  39. Andrade BF, Tannock R (2013) The direct effects of inattention and hyperactivity/impulsivity on peer problems and mediating roles of prosocial and conduct problem behaviors in a community sample of children. J Atten Disord 17(8):670–680 - PubMed
  40. Smaragdi A, Cornwell H, Toschi N, Riccelli R, Gonzalez-Madruga K, Wells A et al (2017) Sex differences in the relationship between conduct disorder and cortical structure in adolescents. J Am Acad Child Adolesc Psychiatry 56(8):703–712 - PubMed
  41. Prendergast BJ, Zucker I (2018) Social behavior: developmental timing defies puberty. Curr Biol: CB 28(9):R553-r555 - PubMed
  42. Girard L-C, Tremblay RE, Nagin D, Côté SM (2019) Development of aggression subtypes from childhood to adolescence: a group-based multi-trajectory modelling perspective. J Abnorm Child Psychol 47(5):825–838 - PubMed
  43. Coccaro EF, McCloskey MS, Fitzgerald DA, Phan KL (2007) Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol Psychiat 62(2):168–178 - PubMed
  44. Besteher B, Squarcina L, Spalthoff R, Bellani M, Gaser C, Brambilla P et al (2017) Brain structural correlates of irritability: findings in a large healthy cohort. Hum Brain Mapp 38(12):6230–6238 - PubMed
  45. Holz NE, Boecker R, Hohm E, Zohsel K, Buchmann AF, Blomeyer D et al (2015) The long-term impact of early life poverty on orbitofrontal cortex volume in adulthood: results from a prospective study over 25 years. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 40(4):996–1004 - PubMed
  46. Murray AL, Eisner M, Obsuth I, Ribeaud D (2017) Situating violent ideations within the landscape of mental health: associations between violent ideations and dimensions of mental health. Psychiatry Res 249:70–77 - PubMed
  47. Wertz J, Agnew-Blais J, Caspi A, Danese A, Fisher HL, Goldman-Mellor S et al (2018) From childhood conduct problems to poor functioning at age 18 years: examining explanations in a longitudinal cohort study. J Am Acad Child Adolesc Psychiatry 57(1):54-60.e54 - PubMed
  48. Leadbeater BJ, Homel J (2015) Irritable and defiant sub-dimensions of ODD: their stability and prediction of internalizing symptoms and conduct problems from adolescence to young adulthood. J Abnorm Child Psychol 43(3):407–421 - PubMed
  49. Wakschlag LS, Perlman SB, Blair RJ, Leibenluft E, Briggs-Gowan MJ, Pine DS (2018) The neurodevelopmental basis of early childhood disruptive behavior: irritable and callous phenotypes as exemplars. Am J Psychiatry 175(2):114–130 - PubMed
  50. Brown BB (2004) Adolescents’ relationships with peers. Handbook of adolescent psychology. 363–394 - PubMed
  51. Steinberg L, Monahan KC (2007) Age differences in resistance to peer influence. Dev Psychol 43(6):1531–1543 - PubMed
  52. Eagly AH, Wood W (2013) The nature-nurture debates: 25 years of challenges in understanding the psychology of gender. Perspect Psychol Sci: J Assoc Psychol Sci 8(3):340–357 - PubMed
  53. Bartels M, Cacioppo JT, van Beijsterveldt TC, Boomsma DI (2013) Exploring the association between well-being and psychopathology in adolescents. Behav Genet 43(3):177–190 - PubMed
  54. Kendler KS, Gardner CO (2014) Sex differences in the pathways to major depression: a study of opposite-sex twin pairs. Am J Psychiatry 171(4):426–435 - PubMed
  55. Nyborg H (2005) Sex-related differences in general intelligence g, brain size, and social status. Personality Individ Differ 39(3):497–509 - PubMed

Publication Types

Grant support