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White matter microstructure of the extended limbic system in male and female youth with conduct disorder

Published online by Cambridge University Press:  30 January 2019

Karen González-Madruga*
Affiliation:
Department of Psychology, University of Southampton, Southampton, UK
Jack Rogers
Affiliation:
School of Psychology and Birmingham University Imaging Centre, University of Birmingham, Birmingham, UK
Nicola Toschi
Affiliation:
Department of Biomedicine and Prevention, University of Rome ‘Tor Vergata’, Rome, Italy
Roberta Riccelli
Affiliation:
Department of Psychology, University of Southampton, Southampton, UK
Areti Smaragdi
Affiliation:
Centre for Addiction and Mental Health, Toronto, Canada
Ignazio Puzzo
Affiliation:
West London Mental Health Trust, Broadmoor High Secure Hospital, London, UK
Roberta Clanton
Affiliation:
School of Psychology and Birmingham University Imaging Centre, University of Birmingham, Birmingham, UK
Jesper Andersson
Affiliation:
FMRIB, John Radcliffe Hospital, University of Oxford, Oxford, UK
Sarah Baumann
Affiliation:
Department of Child and Adolescent Psychiatry, Child Neuropsychology Section, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany
Gregor Kohls
Affiliation:
Department of Child and Adolescent Psychiatry, Child Neuropsychology Section, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany
Nora Raschle
Affiliation:
Department of Child and Adolescent Psychiatry, Psychiatric University Clinics and University of Basel, Basel, Switzerland
Lynn Fehlbaum
Affiliation:
Department of Child and Adolescent Psychiatry, Psychiatric University Clinics and University of Basel, Basel, Switzerland
Willeke Menks
Affiliation:
Department of Child and Adolescent Psychiatry, Psychiatric University Clinics and University of Basel, Basel, Switzerland
Christina Stadler
Affiliation:
Department of Child and Adolescent Psychiatry, Psychiatric University Clinics and University of Basel, Basel, Switzerland
Kerstin Konrad
Affiliation:
Department of Child and Adolescent Psychiatry, Child Neuropsychology Section, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany
Christine M. Freitag
Affiliation:
Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany
Stephane A. De Brito
Affiliation:
School of Psychology and Birmingham University Imaging Centre, University of Birmingham, Birmingham, UK
Edmund Sonuga-Barke
Affiliation:
Child and Adolescent Psychiatry Department, Institute of Psychiatry, Psychology and Neuroscience, Kings College London, London, UK
Graeme Fairchild
Affiliation:
Department of Psychology, University of Bath, Bath, UK
*
Author for correspondence: Karen González-Madruga, E-mail: [email protected]

Abstract

Background

Previous studies of conduct disorder (CD) have reported structural and functional alterations in the limbic system. However, the white matter tracts that connect limbic regions have not been comprehensively studied. The uncinate fasciculus (UF), a tract connecting limbic to prefrontal regions, has been implicated in CD. However, CD-related alterations in other limbic tracts, such as the cingulum and the fornix, have not been investigated. Furthermore, few studies have examined the influence of sex and none have been adequately powered to test whether the relationship between CD and structural connectivity differs by sex. We examined whether adolescent males and females with CD exhibit differences in structural connectivity compared with typically developing controls.

Methods

We acquired diffusion-weighted magnetic resonance imaging data from 101 adolescents with CD (52 females) and 99 controls (50 females). Data were processed for deterministic spherical deconvolution tractography. Virtual dissections of the UF, the three subdivisions of the cingulum [retrosplenial cingulum (RSC), parahippocampal and subgenual cingulum], and the fornix were performed and measures of fractional anisotropy (FA) and hindrance-modulated orientational anisotropy (HMOA) were analysed.

Results

The CD group had lower FA and HMOA in the right RSC tract relative to controls. Importantly, these effects were moderated by sex – males with CD significantly lower FA compared to male controls, whereas CD and control females did not differ.

Conclusions

Our results highlight the importance of considering sex when studying the neurobiological basis of CD. Sex differences in RSC connectivity may contribute to sex differences in the clinical presentation of CD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2019 

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References

Alegria, AA, Radua, J and Rubia, K (2016) Meta-analysis of fMRI studies of disruptive behavior disorders. American Journal of Psychiatry 173, 11191130.Google Scholar
American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Arlington, VA: Washington, DC: American Psychiatric Publishing.Google Scholar
Andershed, HA, Kerr, M, Stattin, H and Levander, S (2002) E. Blaauw and L. Sheridan (eds.) Psychopathic traits in non-referred youths: initial test of a new assessment tool. Psychopaths: Current International Perspectives, 131158. Hague, Netherlands, Elsevier.Google Scholar
Andersson, JLR and Sotiropoulos, SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage 125, 10631078.Google Scholar
Andersson, JLR, Graham, MS, Zsoldos, E and Sotiropoulos, SN (2016) Incorporating outlier detection and replacement into a non-parametric framework for movement and distortion correction of diffusion MR images. NeuroImage 141, 556572.Google Scholar
Aoki, Y, Inokuchi, R, Nakao, T and Yamasue, H (2014) Neural bases of antisocial behavior: a voxel-based meta-analysis. Social Cognitive and Affective Neuroscience 9, 12231231.Google Scholar
Asato, MR, Terwilliger, R, Woo, J and Luna, B (2010) White matter development in adolescence: a DTI study. Cerebral Cortex 20, 21222131.Google Scholar
Auriat, AM, Borich, MR, Snow, NJ, Wadden, KP and Boyd, LA (2015) Comparing a diffusion tensor and non-tensor approach to white matter fiber tractography in chronic stroke. NeuroImage: Clinical 7, 771781.Google Scholar
Barkley, RA, Fischer, M, Smallish, L and Fletcher, K (2004) Young adult follow-up of hyperactive children: antisocial activities and drug use. Journal of Child Psychology and Psychiatry, and Allied Disciplines 45, 195211. Available at http://www.ncbi.nlm.nih.gov/pubmed/14982236.Google Scholar
Basser, PJ, Pajevic, S, Pierpaoli, C, Duda, J and Aldroubi, A (2000) In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine 632, 625632.Google Scholar
Blair, RJ (2008) The amygdala and ventromedial prefrontal cortex: functional contributions and dysfunction in psychopathy. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 363, 25572565.Google Scholar
Broulidakis, MJ, Fairchild, G, Sully, K, Blumensath, T, Darekar, A and Sonuga-Barke, EJS (2016) Reduced default mode connectivity in adolescents with conduct disorder. Journal of the American Academy of Child & Adolescent Psychiatry 55, 800808.Google Scholar
Casey, BJ, Jones, RM and Hare, TA (2008) The adolescent brain. Annals of the New York Academy of Sciences 1124, 111126.Google Scholar
Catani, M and Thiebaut De Schotten, M (2012) Atlas of Human Brain Connections. Oxford University Press. Available at http://books.google.com/books?id=nROILZ9HwEgC&pgis=1.Google Scholar
Catani, M, Dell’ Acqua, F and Thiebaut De Schotten, M (2013) Neuroscience and biobehavioral reviews a revised limbic system model for memory, emotion and behaviour. Neuroscience and Biobehavioral Reviews 37, 17241737.Google Scholar
Craig, MC, Catani, M, Deeley, Q, Latham, R, Daly, E, Kanaan, R and Murphy, DGM (2009) Altered connections on the road to psychopathy. Molecular Psychiatry 14, 946953, 907.Google Scholar
Christiansen, K, Aggleton, JP, Parker, GD, O'Sullivan, MJ, Vann, SD and Metzler-Baddeley, C (2016) The status of the precommissural and postcommissural fornix in normal ageing and mild cognitive impairment: An MRI tractography study. NeuroImage 130, 3547.Google Scholar
Decety, J, Yoder, KJ and Lahey, BB (2015) Sex differences in abnormal white matter development associated with conduct disorder in children. Psychiatry Research – Neuroimaging 233, 269277.Google Scholar
Dell'Acqua, F, Scifo, P, Rizzo, G, Catani, M, Simmons, A, Scotti, G and Fazio, F (2010) A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution. NeuroImage 49, 14461458.Google Scholar
Dell'Acqua, F, Simmons, A, Williams, SCR and Catani, M (2013) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Human Brain Mapping 34, 24642483.Google Scholar
Dunst, B, Benedek, M, Koschutnig, K, Jauk, E and Neubauer, AC (2014) Sex differences in the IQ-white matter microstructure relationship: a DTI study. Brain and Cognition 91, 7178.Google Scholar
Essau, CA, Sasagawa, S and Frick, PJ (2006) Callous-unemotional traits in a community sample of adolescents. Assessment 13, 454469.Google Scholar
Fairchild, G, Hagan, CC, Walsh, ND, Passamonti, L, Calder, AJ and Goodyer, IM (2013) Brain structure abnormalities in adolescent girls with conduct disorder. Journal of Child Psychology and Psychiatry and Allied Disciplines 54, 8695.Google Scholar
Fairchild, G, Toschi, N, Hagan, CC, Goodyer, IM, Calder, AJ and Passamonti, L (2015) Cortical thickness, surface area, and folding alterations in male youths with conduct disorder and varying levels of callous-unemotional traits. NeuroImage: Clinical 8, 253260.Google Scholar
Finger, EC, Marsh, A, Blair, KS, Majestic, C, Evangelou, I, Gupta, K and Blair, RJ (2012) Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits. Psychiatry Research 202, 239244.Google Scholar
Haney-Caron, E, Caprihan, A and Stevens, MC (2014) DTI-measured white matter abnormalities in adolescents with conduct disorder. Journal of Psychiatric Research 48, 111120.Google Scholar
Harsan, LA, Poulet, P, Guignard, B, Steibel, J, Parizel, N, de Sousa, PL and Ghandour, MS (2006) Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. Journal of Neuroscience Research 83, 392402.Google Scholar
Herpertz, SC, Huebner, T, Marx, I, Vloet, TD, Fink, GR, Stoecker, T and 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, DK, Christiansen, KF, Chapman, RJ and Aggleton, JP (2013) Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: implications for neuropsychological investigations. Neuropsychologia 51, 6778.Google Scholar
Kaufman, J, Birmaher, B, Perel, J, Dahl, RE, Moreci, P, Nelson, B, … Ryan, ND (1997) The corticotropin-releasing hormone challenge in depressed abused, depressed nonabused, and normal control children. Biological Psychiatry 42, 669679.Google Scholar
Leech, R, Braga, R and Sharp, DJ (2012) Echoes of the brain within the posterior cingulate cortex. Journal of Neuroscience 32, 215222.Google Scholar
Menks, WM, Furger, R, Lenz, C, Fehlbaum, LV, Stadler, C and Raschle, NM (2017) Microstructural white matter alterations in the corpus callosum of girls with conduct disorder. Journal of the American Academy of Child & Adolescent Psychiatry 56, 258265. e1.Google Scholar
Passamonti, L, Fairchild, G, Fornito, A, Goodyer, IM, Nimmo-Smith, I, Hagan, CC and Calder, AJ (2012) Abnormal anatomical connectivity between the amygdala and orbitofrontal cortex in conduct disorder. PLoS ONE 7, e48789.Google Scholar
Puzzo, I, Seunarine, K, Sully, K, Darekar, A, Clark, C, Sonuga-Barke, EJS and Fairchild, G (2018) Altered white-matter microstructure in conduct disorder is specifically associated with elevated callous-unemotional traits. Journal of Abnormal Child Psychology 46, 14511466.Google Scholar
Raffelt, DA, Smith, RE, Ridgway, GR, Tournier, J-D, Vaughan, DN, Rose, S and Connelly, A (2015) Connectivity-based fixel enhancement: whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres. NeuroImage 117, 4055.Google Scholar
Raschle, NM, Menks, WM, Fehlbaum, LV, Tshomba, E and Stadler, C (2015) Structural and functional alterations in right dorsomedial prefrontal and left insular cortex co-localize in adolescents with aggressive behaviour: an ALE meta-analysis. PLoS ONE 10, 124.Google Scholar
Rogers, JC and De Brito, SA (2016) Cortical and subcortical gray matter volume in youths with conduct problems. JAMA Psychiatry 73, 64.Google Scholar
Rolls, ET (2004) The functions of the orbitofrontal cortex. Brain and Cognition 55, 1129.Google Scholar
Rolls, ET (2015) Limbic systems for emotion and for memory, but no single limbic system. Cortex 62, 119157.Google Scholar
Rojkova, K, Volle, E, Urbanski, M, Humbert, F, Dell'Acqua, F, Thiebaut de Schotten, M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain and Cognition 221, 17511766.Google Scholar
Sarkar, S, Craig, MC, Catani, M, Dell ’Acqua, F, Fahy, T, Deeley, Q and Murphy, DGM (2013) Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study. Psychological Medicine 43, 401411.Google Scholar
Sethi, A, Gregory, S, Dell'Acqua, F, Periche Thomas, E, Simmons, A, Murphy, DGM and Craig, MC (2015) Emotional detachment in psychopathy: involvement of dorsal default-mode connections. Cortex 62, 1119.Google Scholar
Sethi, A, Sarkar, S, Dell'Acqua, F, Viding, E, Catani, M, Murphy, DGM and Craig, MC (2018) Anatomy of the dorsal default-mode network in conduct disorder: association with callous-unemotional traits. Developmental Cognitive Neuroscience 30, 8792.Google Scholar
Sidlauskaite, J, González-Madruga, K, Smaragdi, A, Riccelli, R, Puzzo, I, Batchelor, M and Fairchild, G (2018) Sex differences in risk-based decision making in adolescents with conduct disorder. European Child and Adolescent Psychiatry 27, 11331142.Google Scholar
Simmonds, DJ, Hallquist, MN, Asato, M and Luna, B (2014) Developmental stages and sex differences of white matter and behavioral development through adolescence: A longitudinal diffusion tensor imaging (DTI) study. NeuroImage 92, 356368.Google Scholar
Smaragdi, A, Cornwell, H, Toschi, N, Riccelli, R, Gonzalez-Madruga, K, Wells, A and Fairchild, G (2017) Sex differences in the relationship between conduct disorder and cortical structure in adolescents. Journal of the American Academy of Child and Adolescent Psychiatry 56, 703712.Google Scholar
Stieltjes, B, Brunner, RM, Fritzsche, KH and Laun, FB (2013) Diffusion Tensor Imaging. Berlin, Heidelberg: Springer Berlin Heidelberg.Google Scholar
Van Casteren, M and Davis, MH (2007) Match: a program to assist in matching the conditions of factorial experiments. Behavior Research Methods 39, 973978.Google Scholar
Vanderauwera, J, Vandermosten, M, Dell'Acqua, F, Wouters, J and Ghesquière, P (2015) Disentangling the relation between left temporoparietal white matter and reading: a spherical deconvolution tractography study. Human Brain Mapping 36, 32733287.Google Scholar
Wang, Y, Horst, KK, Kronenberger, WG, Hummer, TA, Mosier, KM, Kalnin, AJ and Mathews, VP (2012) White matter abnormalities associated with disruptive behavior disorder in adolescents with and without attention-deficit/hyperactivity disorder. Psychiatry Research – Neuroimaging 202, 245251.Google Scholar
Wechsler, D (1999) Wechsler Abbreviated Scale of Intelligence (WASI). Psychological Corporation, 1.Google Scholar
Wechsler, D (2003) Wechsler Intelligence Scale for Children–Fourth Edition (WISC-IV). NCS Pearson, 4.Google Scholar
White, SF, Clanton, R, Brislin, SJ, Meffert, H, Hwang, S, Sinclair, S and Blair, RJ (2014) Reward: empirical contribution. Temporal discounting and conduct disorder in adolescents. Journal of Personality Disorders 28, 518.Google Scholar
Zhang, J, Gao, J, Shi, H, Huang, B, Wang, X, Situ, W and Yao, S (2014) Sex differences of uncinate fasciculus structural connectivity in individuals with conduct disorder. BioMed Research International 14, 9.Google Scholar
Zhou, J, Yao, N, Fairchild, G, Cao, X, Zhang, Y, Xiang, Y-T and Wang, X (2016) Disrupted default mode network connectivity in male adolescents with conduct disorder. Brain Imaging and Behavior 10, 9951003.Google Scholar
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