[Skip to Content]
[Skip to Content Landing]
Original Investigation
October 2018

Examination of the Neural Basis of Psychoticlike Experiences in Adolescence During Reward Processing

Author Affiliations
  • 1Cognition Schizophrenia and Imaging Laboratory, Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
  • 2Department of Psychosis Studies, Institute of Psychiatry Psychology and Neuroscience, King’s College London, London, United Kingdom
  • 3Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
  • 4Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
  • 5Department of Systems Neuroscience, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
  • 6Centre for Population Neuroscience and Stratified Medicine, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
  • 7Medical Research Council, Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
  • 8Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
  • 9Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany
  • 10NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France
  • 11Department of Psychiatry, University of Vermont, Burlington
  • 12Department of Psychology, University of Vermont, Burlington
  • 13Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom
  • 14Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin, Germany
  • 15Physikalisch-Technische Bundesanstalt, Berlin, Germany
  • 16Institut National de la Santé et de la Recherche Médicale, Neuroimaging & Psychiatry, University Paris Saclay, DIGITEO Labs, Gif sur Yvette, France
  • 17Institut National de la Santé et de la Recherche Médicale, Neuroimaging & Psychiatry, University Paris Sud – Paris Saclay, University Paris Descartes, Paris, France
  • 18Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris, France
  • 19Psychiatry Department, Orsay Hospital, Orsay, France
  • 20Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen, Germany
  • 21Clinic for Child and Adolescent Psychiatry, Medical University of Vienna, Vienna, Austria
  • 22Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
  • 23School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland
JAMA Psychiatry. 2018;75(10):1043-1051. doi:10.1001/jamapsychiatry.2018.1973
Key Points

Question  Are psychoticlike experiences in adolescents associated with altered prefrontal and striatal activation during reward processing?

Findings  In this cohort study of 298 adolescents, those with an elevated rate of psychoticlike experiences at age 14 years demonstrated reduced activation in prefrontal and limbic cortical areas during reward processing compared with adolescents with no psychoticlike experiences. However, by age 19 years, the group with the elevated rate of psychoticlike experiences showed differentially increased activation of the right prefrontal cortex and reduced activation of dorsal striatum.

Meaning  Adolescents with an elevated rate of psychoticlike experiences show differential activation in frontostriatal brain areas engaged during reward processing compared with control adolescents; given the nonclinical nature of the sample, the increase in prefrontal cortical activation from early to late adolescence may reflect a compensatory cognitive mechanism in the presence of abnormal striatal reward processing to contextualize these abnormal experiences.

Abstract

Importance  Psychoticlike experiences (PLEs) are subclinical manifestations of psychotic symptoms and may reflect an increased vulnerability to psychotic disorders. Contemporary models of psychosis propose that dysfunctional reward processing is involved in the cause of these clinical illnesses.

Objective  To examine the neuroimaging profile of healthy adolescents at 14 and 19 years old points with PLEs, using a reward task.

Design, Setting, and Participants  A community-based cohort study, using both a cross-sectional and longitudinal design, was conducted in academic centers in London, Nottingham, United Kingdom, and Dublin, Ireland; Paris, France; and Berlin, Hamburg, Mannheim, and Dresden, Germany. A group of 1434 healthy adolescent volunteers was evaluated, and 2 subgroups were assessed at ages 14 and 19 years. Those who scored as either high or low PLE (based on the upper and lower deciles) on the Community Assessment of Psychic Experiences Questionnaire (CAPE-42) at age 19 years were included in the analysis. The study was conducted from January 1, 2016, to January 1, 2017.

Main Outcomes and Measures  Participants were assessed at age 14 and 19 year points using functional magnetic resonance imaging while performing a monetary incentive delay reward task. A first-level model focused on 2 predefined contrasts of anticipation and feedback of a win. The second-level analysis examined activation within the reward network using an a priori–defined region of interest approach. The main effects of group, time, and their interaction on brain activation were examined.

Results  Of the 1434 adolescents, 2 groups (n = 149 each) (high PLEs, n = 149, 50 [33.6%] male; low PLEs, n = 149, 84 [56.4%] male) were compared at ages 14 and 19 years. Two regions within the left and right middle frontal gyri showed a main effect of time on brain activation (F1, 93 = 5.559; P = .02; F1, 93 = 5.009; P = .03, respectively); there was no main effect of group. One region within the right middle frontal gyrus demonstrated a significant time × group interaction (F1, 93 = 7.448; P = .01).

Conclusion and Relevance  The findings are consistent with evidence implicating alterations in prefrontal and striatal function during reward processing in the etiology of psychosis. Given the nature of this nonclinical sample this may reflect a combination of aberrant salience yielding abnormal experiences and a compensatory cognitive control mechanism necessary to contextualize them.

×