Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T17:35:10.958Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of childhood trauma on left inferior frontal gyrus function during response inhibition across psychotic disorders

Published online by Cambridge University Press:  10 October 2017

Y. Quidé ,
N. O'Reilly ,
O. J. Watkeys ,
V. J. Carr  and
M. J. Green
Y. Quidé
Affiliation:
School of Psychiatry, University of New South Wales, Randwick, NSW, Australia Neuroscience Research Australia, Randwick, NSW, Australia
N. O'Reilly
Affiliation:
School of Psychiatry, University of New South Wales, Randwick, NSW, Australia
O. J. Watkeys
Affiliation:
School of Psychiatry, University of New South Wales, Randwick, NSW, Australia Neuroscience Research Australia, Randwick, NSW, Australia
V. J. Carr
Affiliation:
School of Psychiatry, University of New South Wales, Randwick, NSW, Australia Neuroscience Research Australia, Randwick, NSW, Australia Department of Psychiatry, School of Clinical Sciences, Monash University, Clayton, VIC, Australia
M. J. Green*
Affiliation:
School of Psychiatry, University of New South Wales, Randwick, NSW, Australia Neuroscience Research Australia, Randwick, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW, Australia ARC Centre for Cognition and its Disorders (CCD), Macquarie University, Sydney, NSW, Australia
*
Author for correspondence: Associate Professor M. J. Green, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Childhood trauma is a risk factor for psychosis. Deficits in response inhibition are common to psychosis and trauma-exposed populations, and associated brain functions may be affected by trauma exposure in psychotic disorders. We aimed to identify the influence of trauma-exposure on brain activation and functional connectivity during a response inhibition task.

Methods

We used functional magnetic resonance imaging to examine brain function within regions-of-interest [left and right inferior frontal gyrus (IFG), right dorsolateral prefrontal cortex, right supplementary motor area, right inferior parietal lobule and dorsal anterior cingulate cortex], during the performance of a Go/No-Go Flanker task, in 112 clinical cases with psychotic disorders and 53 healthy controls (HCs). Among the participants, 71 clinical cases and 21 HCs reported significant levels of childhood trauma exposure, while 41 clinical cases and 32 HCs did not.

Results

In the absence of effects on response inhibition performance, childhood trauma exposure was associated with increased activation in the left IFG, and increased connectivity between the left IFG seed region and the cerebellum and calcarine sulcus, in both cases and healthy individuals. There was no main effect of psychosis, and no trauma-by-psychosis interaction for any other region-of-interest. Within the clinical sample, the effects of trauma-exposure on the left IFG activation were mediated by symptom severity.

Conclusions

Trauma-related increases in activation of the left IFG were not associated with performance differences, or dependent on clinical diagnostic status; increased IFG functionality may represent a compensatory (overactivation) mechanism required to exert adequate inhibitory control of the motor response.

Keywords

Childhood traumafMRIGo/No-Go Flanker taskpsychosis
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 9 , July 2018 , pp. 1454 - 1463
Copyright
Copyright © Cambridge University Press 2017 

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

Aas, M et al. (2011) Childhood trauma and cognitive function in first-episode affective and non-affective psychosis. Schizophrenia Research 129, 12–19.CrossRefGoogle ScholarPubMed
Abbott, CC et al. (2013) Antipsychotic drug effects in schizophrenia: a review of longitudinal FMRI investigations and neural interpretations. Current Medicinal Chemistry 20, 428–437.Google ScholarPubMed
Alsawy, S et al. (2015) Psychotic experiences and PTSD: exploring associations in a population survey. Psychological Medicine 45, 2849–2859.CrossRefGoogle Scholar
Alvarez, MJ et al. (2011) Prevalence and clinical impact of childhood trauma in patients with severe mental disorders. Journal of Nervous and Mental Disease 199, 156–161.CrossRefGoogle ScholarPubMed
Aron, AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 69, e55–e68.CrossRefGoogle ScholarPubMed
Aron, AR, Robbins, TW and Poldrack, RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends in Cognitive Sciences 18, 177–185.Google Scholar
Berk, M et al. (2007) The bipolar depression rating scale (BDRS): its development, validation and utility. Bipolar Disorders 9, 571–579.Google Scholar
Bernstein, DP et al. (2003) Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse and Neglect 27, 169–190.Google Scholar
Blasi, G et al. (2006) Brain regions underlying response inhibition and interference monitoring and suppression. European Journal of Neuroscience 23, 1658–1664.Google Scholar
Boehler, CN et al. (2010) Pinning down response inhibition in the brain – conjunction analyses of the Stop-signal task. NeuroImage 52, 1621–1632.CrossRefGoogle ScholarPubMed
Brett, M et al. (2002) Region of interest analysis using an SPM toolbox. In 8th International Conference on Functional Mapping of the Human Brain. NeuroImage: Sendai, Japan.Google Scholar
Cancel, A et al. (2015) Childhood neglect predicts disorganization in schizophrenia through grey matter decrease in dorsolateral prefrontal cortex. Acta Psychiatrica Scandinavica 132, 244–256.Google Scholar
Carrion, VG et al. (2008) Posttraumatic stress symptoms and brain function during a response-inhibition task: an fMRI study in youth. Depression and Anxiety 25, 514–526.Google Scholar
Castle, DJ et al. (2006) The diagnostic interview for psychoses (DIP): development, reliability and applications. Psychological Medicine 36, 69–80.CrossRefGoogle ScholarPubMed
Criaud, M and Boulinguez, P (2013) Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review. Neuroscience & Biobehavioral Reviews 37, 11–23.Google Scholar
Duhig, M et al. (2015) The prevalence and correlates of childhood trauma in patients with early psychosis. Australian and New Zealand Journal of Psychiatry 49, 651–659.CrossRefGoogle ScholarPubMed
Faul, F et al. (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behavior Research Methods 41, 1149–1160.Google Scholar
Faul, F et al. (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39, 175–191.Google Scholar
Fusar-Poli, P et al. (2013) Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neuroscience & Biobehavioral Reviews 37, 1680–1691.Google Scholar
Gibson, LE, Alloy, LB and Ellman, LM (2016) Trauma and the psychosis spectrum: a review of symptom specificity and explanatory mechanisms. Clinical Psychology Review 49, 92–105.Google Scholar
Green, MJ et al. (2014) Stress, schizophrenia and bipolar disorder. In Behavioral Neurobiology of Stress-Related Disorders (ed. Pariante, M. C., Lapiz-Bluhm, D. M.), pp. 217–235. Springer Berlin Heidelberg: Berlin, Heidelberg.Google Scholar
Gu, X et al. (2013) Anterior insular cortex and emotional awareness. Journal of Comparative Neurology 521, 3371–3388.Google Scholar
Hardy, A et al. (2016) Psychological mechanisms mediating effects between trauma and psychotic symptoms: the role of affect regulation, intrusive trauma memory, beliefs, and depression. Schizophrenia Bulletin 42, S34–S43.Google Scholar
Hart, H and Rubia, K (2012) Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience 6, 52.CrossRefGoogle ScholarPubMed
Hayes, AF (2013) Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach. Guilford Press, New York, USA.Google Scholar
Hill, SK et al. (2013) Neuropsychological impairments in schizophrenia and psychotic bipolar disorder: findings from the bipolar-schizophrenia network on intermediate phenotypes (B-SNIP) study. American Journal of Psychiatry 170, 1275–1284.Google Scholar
Ho, BC et al. (2011) Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Archives of General Psychiatry 68, 128–137.Google Scholar
Isvoranu, AM et al. (2017) A network approach to psychosis: pathways between childhood trauma and psychotic symptoms. Schizophrenia Bulletin 43, 187–196.Google Scholar
Ivleva, EI et al. (2012) Cognitive endophenotypes of psychosis within dimension and diagnosis. Psychiatry Research 196, 38–44.Google Scholar
Kay, SR, Opler, LA and Lindenmayer, J-P (1989) The positive and negative syndrome scale (PANSS): rationale and standardisation. The British Journal of Psychiatry 155, 59–65.CrossRefGoogle Scholar
Keren-Happuch, E et al. (2014) A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Human Brain Mapping 35, 593–615.Google Scholar
Leucht, S et al. (2003) New generation antipsychotics versus low-potency conventional antipsychotics: a systematic review and meta-analysis. Lancet 361, 1581–1589.Google Scholar
Lim, L et al. (2015) Neural correlates of error processing in young people with a history of severe childhood abuse: an fMRI study. American Journal of Psychiatry 172, 892–900.CrossRefGoogle ScholarPubMed
Lim, L, Radua, J and Rubia, K (2014) Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis. American Journal of Psychiatry 171, 854–863.Google Scholar
Loughland, C et al. (2010) Australian Schizophrenia Research Bank: a database of comprehensive clinical, endophenotypic and genetic data for aetiological studies of schizophrenia. Australian and New Zealand Journal of Psychiatry 44, 1029–1035.Google Scholar
Lovibond, SH and Lovibond, PF (1995) The DASS: Manual for the Depression, Anxiety Stress Scales, 2nd edn. Psychology Foundation of Australia, Sydney, NSW, Australia.Google Scholar
Lysaker, PH et al. (2001) Neurocognitive and symptom correlates of self-reported childhood sexual abuse in schizophrenia spectrum disorders. Annals of Clinical Psychiatry 13, 89–92.Google Scholar
McGuffin, P and Farmer, A (1991) A polydiagnostic application of operational criteria in studies of psychotic illness: development and validation of the OPCRIT system. Archives of General Psychiatry 48, 764–770.Google Scholar
McLaren, DG et al. (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61, 1277–1286.Google Scholar
Mitchell, PB et al. (2009) Characteristics of bipolar disorder in an Australian specialist outpatient clinic: comparison across large datasets. Australian and New Zealand Journal of Psychiatry 43, 1009–1017.CrossRefGoogle Scholar
Moncrieff, J and Leo, J (2010) A systematic review of the effects of antipsychotic drugs on brain volume. Psychological Medicine 40, 1409–1422.Google Scholar
Montgomery, P and Asberg, B (1979) A new depression scale designed to be sensitive to change. The British Journal of Psychiatry 134, 382–389.Google Scholar
Mørkved, N et al. (2017) Childhood trauma in schizophrenia spectrum disorder as compared to other mental health disorders. Psychosis 9, 48–56.Google Scholar
Morrison, AP (2001) The interpretation of intrusions in psychosis: an integrative cognitive approach to hallucinations and delusions. Behavioural and Cognitive Psychotherapy 29, 257–276.CrossRefGoogle Scholar
Mueller, SC et al. (2010) Early-life stress is associated with impairment in cognitive control in adolescence: an fMRI study. Neuropsychologia 48, 3037–3044.Google Scholar
Oldfield, RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Peters, ER et al. (2000) The relationship between cognitive inhibition and psychotic symptoms. Journal of Abnormal Psychology 109, 386–395.Google Scholar
Powers, A et al. (2016) Childhood trauma, PTSD, and psychosis: findings from a highly traumatized, minority sample. Child Abuse and Neglect 58, 111–118.Google Scholar
Quidé, Y et al. (2017) Effects of childhood trauma on working memory in affective and non-affective psychotic disorders. Brain Imaging Behavior 11, 722–735.Google Scholar
Read, J et al. (2014) The traumagenic neurodevelopmental model of psychosis revisited. Neuropsychiatry 4, 65–79.Google Scholar
Reichenberg, A et al. (2009) Neuropsychological function and dysfunction in schizophrenia and psychotic affective disorders. Schizophrenia Bulletin 35, 1022–1029.CrossRefGoogle ScholarPubMed
Roberts, G et al. (2013) Reduced inferior frontal gyrus activation during response inhibition to emotional stimuli in youth at high risk of bipolar disorder. Biological Psychiatry 74, 55–61.Google Scholar
Sambataro, F et al. (2013) Altered cerebral response during cognitive control: a potential indicator of genetic liability for schizophrenia. Neuropsychopharmacology 38, 846–853.Google Scholar
Shannon, C et al. (2011) The association between childhood trauma and memory functioning in schizophrenia. Schizophrenia Bulletin 37, 531–537.Google Scholar
Sheehan, DV et al. (1998) The mini-international neuropsychiatric interview (MINI): the development and validation of a structured diagnostic interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 22–33.Google Scholar
Sheffield, JM et al. (2013) Reduced gray matter volume in psychotic disorder patients with a history of childhood sexual abuse. Schizophrenia Research 143, 185–191.Google Scholar
Stoodley, CJ and Schmahmann, JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage 44, 489–501.Google Scholar
Swick, D, Ashley, V and Turken, AU (2008) Left inferior frontal gyrus is critical for response inhibition. BMC Neuroscience 9, 102.CrossRefGoogle ScholarPubMed
Teicher, MH and Samson, JA (2013) Childhood maltreatment and psychopathology: a case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. American Journal of Psychiatry 170, 1114–1133.Google Scholar
Teicher, MH et al. (2016) The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience 17, 652–666.Google Scholar
Uddin, LQ (2015) Salience processing and insular cortical function and dysfunction. Nature Reviews Neuroscience 16, 55–61.Google Scholar
van den Berg, DP et al. (2015) Prolonged exposure vs eye movement desensitization and reprocessing vs waiting list for posttraumatic stress disorder in patients with a psychotic disorder: a randomized clinical trial. JAMA Psychiatry 72, 259–267.Google Scholar
van Haren, NE et al. (2011) Changes in cortical thickness during the course of illness in schizophrenia. Archives of General Psychiatry 68, 871–880.Google Scholar
Varese, F et al. (2012) Childhood adversities increase the risk of psychosis: a meta-analysis of patient-control, prospective- and cross-sectional cohort studies. Schizophrenia Bulletin 38, 661–671.Google Scholar
Wechsler, D (1999) Wechsler Abbreviated Scale of Intelligence (WASI). The Psychological Corporation: New York.Google Scholar
Welander-Vatn, A et al. (2013) The neural correlates of cognitive control in bipolar I disorder: an fMRI study of medial frontal cortex activation during a Go/No-go task. Neuroscience Letters 549, 51–56.Google Scholar
WHO (2008) ICD-10: International Statistical Classification of Diseases and Related Health Problems, 10th Rev. edn. World Health Organization: New York.Google Scholar
Woods, SW (2003) Chlorpromazine equivalent doses for the newer atypical antipsychotics. Journal of Clinical Psychiatry 64, 663–667.Google Scholar
Young, RC et al. (1978) A rating scale for mania: reliability, validity, and sensitivity. The British Journal of Psychiatry 133, 429–435.Google Scholar
Supplementary material: File

Quidé et al supplementary material

Quidé et al supplementary material 1

Download Quidé et al supplementary material(File)
File 92.6 KB