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Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study

Published online by Cambridge University Press:  23 May 2012

S. Sarkar ,
M. C. Craig ,
M. Catani ,
F. Dell'Acqua ,
T. Fahy ,
Q. Deeley  and
D. G. M. Murphy
S. Sarkar*
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK
M. C. Craig
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK
M. Catani
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK
F. Dell'Acqua
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK
T. Fahy
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK
Q. Deeley
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK
D. G. M. Murphy
Affiliation:
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, King's College London, London, UK NIHR Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust and Institute of Psychiatry, King's College London, UK
*
*Address for correspondence: Ms. S. Sarkar, King's College London, Institute of Psychiatry, Department of Forensic and Neurodevelopmental Science, PO Box 50, De Crespigny Park, London SE5 8AF, UK. (Email: [email protected])
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Abstract

Background

Children with conduct disorder (CD) are at increased risk of developing antisocial personality disorder (ASPD) and psychopathy in adulthood. The biological basis for this is poorly understood. A preliminary diffusion tensor magnetic resonance imaging (DT-MRI) study of psychopathic antisocial adults reported significant differences from controls in the fractional anisotropy (FA) of the uncinate fasciculus (UF), a white-matter tract that connects the amygdala to the frontal lobe. However, it is unknown whether developmental abnormalities are present in the UF of younger individuals with CD.

Method

We used DT-MRI tractography to investigate, for the first time, the microstructural integrity of the UF in adolescents with CD, and age-related differences in this tract. We compared FA and perpendicular diffusivity of the UF in 27 adolescents with CD and 16 healthy controls (12 to 19 years old) who did not differ significantly in age, IQ or substance use history. To confirm that these findings were specific to the UF, the same measurements were extracted from two non-limbic control tracts. Participants in the CD group had a history of serious aggressive and violent behaviour, including robbery, burglary, grievous bodily harm and sexual assault.

Results

Individuals with CD had a significantly increased FA (p = 0.006), and reduced perpendicular diffusivity (p = 0.002), in the left UF. Furthermore, there were significant age-related between-group differences in perpendicular diffusivity of the same tract (Zobs = 2.40, p = 0.01). Controls, but not those with CD, showed significant age-related maturation. There were no significant between-group differences in any measure within the control tracts.

Conclusions

Adolescents with CD have significant differences in the ‘connectivity’ and maturation of UF.

Keywords

Conduct disorderdiffusion tensor imagingneuroimagingpsychopathyuncinate fasciculuswhite matter
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 2 , February 2013 , pp. 401 - 411
Copyright
Copyright © Cambridge University Press 2012

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References

Adolphs, R, Tranel, D, Damasio, AR (1998). The human amygdala in social judgment. Nature 393, 470–474.CrossRefGoogle ScholarPubMed
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text revision (DSM-IV-TR). American Psychiatric Association: Washington, DC.Google Scholar
Basser, PJ, Pjevic, S, Pierpaoli, C, Duda, J, Aldoubi, A (2000). In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine 44, 625–632.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Beaulieu, C (2009). The biological basis of diffusion anisotropy. In Diffusion MRI: From Quantitative Measurement to In Vivo Neuroanatomy (ed. Johansen-Berg, H. and Behrens, T. E. J.), pp. 105–126. Elsevier: London.CrossRefGoogle Scholar
Bengetsson, SL, Nagy, Z, Skare, S, Forsman, L, Forssberg, H, Ullen, F (2005). Extensive piano practicing has regionally specific effects on white matter development. Nature Neuroscience 8, 1148–1150.CrossRefGoogle Scholar
Berns, GS, Moore, S, Capra, CM, Berns, GS, Moore, S, Capra, CM (2009). Adolescent engagement in dangerous behaviors is associated with increased white matter maturity of frontal cortex. PLoS ONE 4, e6773.CrossRefGoogle ScholarPubMed
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, 2557–2565.CrossRefGoogle ScholarPubMed
Blair, RJ, Colledge, E, Murray, L, Mitchell, DG (2001). A selective impairment in the processing of sad and fearful expressions in children with psychopathic tendencies. Journal of Abnormal Child Psychology 29, 491–498.CrossRefGoogle ScholarPubMed
Blair, RJ, Peschardt, KS, Budhani, S, Mitchell, DG, Pine, DS, Blair, RJR, Mitchell, DGV (2006). The development of psychopathy. Journal of Child Psychology and Psychiatry, and Allied Disciplines 47, 262–276.CrossRefGoogle ScholarPubMed
Brower, MC, Price, BH (2001). Neuropsychiatry of frontal lobe dysfunction in violent and criminal behaviour: a critical review. Journal of Neurology, Neurosurgery, and Psychiatry 71, 720–726.CrossRefGoogle ScholarPubMed
Budhani, S, Blair, RJ, Blair, RJR (2005). Response reversal and children with psychopathic tendencies: success is a function of salience of contingency change. Journal of Child Psychology and Psychiatry, and Allied Disciplines 46, 972–981.CrossRefGoogle ScholarPubMed
Budhani, S, Richell, RA, Blair, RJ, Budhani, S, Richell, RA, Blair, RJR (2006). Impaired reversal but intact acquisition: probabilistic response reversal deficits in adult individuals with psychopathy. Journal of Abnormal Psychology 115, 552–558.CrossRefGoogle ScholarPubMed
Bussing, R, Grudnic, J, Mason, D, Wasiak, M, Leonard, C (2002). ADHD and conduct disorder: an MRI study in a community sample. World Journal of Psychiatry 3, 216–220.Google Scholar
Catani, M, Howard, RJ, Pajevic, S, Jones, DK (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17, 77–94.CrossRefGoogle ScholarPubMed
Catani, M, Thiebaut de Schotten, M (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44, 1105–1132.CrossRefGoogle ScholarPubMed
Chang, LC, Jones, DK, Pierpaoli, C (2005). RESTORE: robust estimation of tensors by outlier rejection. Magnetic Resonance in Medicine 53, 1088–1095.CrossRefGoogle ScholarPubMed
Choi, J, Jeong, BS, Rohan, ML, Polcari, AM, Teicher, MH (2009). Preliminary evidence for white matter tract abnormalities in young adults exposed to parental verbal abuse. Biological Psychiatry 65, 227–234.CrossRefGoogle ScholarPubMed
Christian, RE, Frick, PJ, Hill, NL, Tyler, L, Frazer, DR (1997). Psychopathy and conduct problems in children: II. Implications for subtyping children with conduct problems. Journal of the American Academy of Child and Adolescent Psychiatry 36, 233–241.CrossRefGoogle ScholarPubMed
Craig, MC, Catani, M, Deeley, Q, Latham, R, Daly, E, Kanaan, R, Picchioni, R, McGuire, PK, Fahy, T, Murphy, DG (2009). Altered connections on the road to psychopathy. Molecular Psychiatry 14, 946–953.CrossRefGoogle ScholarPubMed
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, 280–281.CrossRefGoogle Scholar
De Brito, SA, McCrory, EJ, Mechelli, A, Wilke, M, Jones, AP, Hodgins, S, Viding, E (2011). Small, but not perfectly formed: decreased white matter concentration in boys with psychopathic tendencies. Molecular Psychiatry 16, 476–477.CrossRefGoogle Scholar
De Brito, SA, Mechelli, A, Wilke, M, Laurens, KR, Jones, AP, Barker, GJ, Hodgins, GJ, Viding, E (2009). Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132, 843–852.CrossRefGoogle ScholarPubMed
Deeley, Q, Daly, E, Surguladze, S, Tunstall, N, Mezey, G, Beer, D, Ambikapathy, A, Robertson, D, Giampietro, V, Brammer, MJ, Clarke, A, Dowsett, J, Fahy, T, Phillips, ML, Murphy, DG (2006). Facial emotion processing in criminal psychopathy. Preliminary functional magnetic resonance imaging study. British Journal of Psychiatry 189, 533–539.CrossRefGoogle ScholarPubMed
de Oliveira-Souza, R, Hare, RD, Bramati, IE, Garrido, GJ, Azevedo Ignácio, F, Tovar-Moll, F, Moll, J (2008). Psychopathy as a disorder of the moral brain: fronto-temporo-limbic grey matter reductions demonstrated by voxel-based morphometry. NeuroImage 40, 1202–1213.CrossRefGoogle ScholarPubMed
Eluvathingal, TJ, Chugani, HT, Behen, ME, Juhasz, C, Muzik, O, Maqbool, M, Chugani, DC, Makki, M (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics 117, 2093–2100.CrossRefGoogle ScholarPubMed
Fahim, C, He, Y, Yoon, U, Chen, J, Evans, AC, Perusse, D (2011). Neuroanatomy of childhood disruptive behavior disorders. Aggressive Behavior 37, 1–12.CrossRefGoogle ScholarPubMed
Fairchild, G, Passamonti, L, Hurford, G, Hagan, CC, von dem Hagen, EAH, van Goozen, SHM, Goodyer, IM, Calder, AJ (2011). Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. American Journal of Psychiatry 168, 624–633.CrossRefGoogle ScholarPubMed
Finger, EC, Marsh, AA, Mitchell, DG, Reid, ME, Sims, C, Budhani, S, Kosson, DS, Chen, G, Towbin, KE, Leibenluft, E, Pine, DS, Blair, JR (2008). Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning. Archives of General Psychiatry 65, 586–594.CrossRefGoogle ScholarPubMed
Forth, AE, Kosson, D, Hare, RD (2003). Hare Psychopathy Checklist: Youth Version (PCL:YV). Multi-Health Systems Inc.: Toronto, Canada.Google Scholar
Frick, PJ (1998). Conduct Disorders and Severe Antisocial Behavior. Plenum: New York.CrossRefGoogle Scholar
Frick, PJ, Hare, RD (2001). The Antisocial Process Screening Version (ASPD). Multi-Health Systems Inc.: Toronto, Canada.Google Scholar
Gaffan, D, Eacott, MJ (1995). Uncinate fascicle section leaves delayed matching-to-sample intact, with both large and small stimulus sets. Experimental Brain Research 105, 175–185.CrossRefGoogle ScholarPubMed
Gelhorn, HL, Sakai, JT, Price, RK, Crowley, TJ (2007). DSM-IV conduct disorder criteria as predictors of antisocial personality disorder. Comprehensive Psychiatry 48, 529–538.CrossRefGoogle ScholarPubMed
Goodman, R (1999). The extended version of the strengths and difficulties questionnaire as a guide to child psychiatric cases and consequent burden. Journal of Child Psychology and Psychiatry 40, 779–799.CrossRefGoogle Scholar
Gutnikov, SA, Ma, YY, Gaffan, D (1997). Temporo-frontal disconnection impairs visual-visual paired association learning but not configural learning in Macaca monkeys. European Journal of Neuroscience 9, 1524–1529.CrossRefGoogle Scholar
Hare, RD (1991). The Hare Psychopathy Checklist – Revised, 1st edn.Multi-Health Systems, Inc.: Toronto, Ontario.Google Scholar
Horsfield, MA, Jones, DK (2002). Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR in Biomedicine 15, 570–577.CrossRefGoogle ScholarPubMed
Huebner, T, Vloet, TD, Marx, I, Konrad, K, Fink, GR, Herpertz, SC, Herpertz-Dahlmann, B (2008). Morphometric brain abnormalities in boys with conduct disorder. Journal of the American Academy of Child and Adolescent Psychiatry 47, 540–547.CrossRefGoogle ScholarPubMed
Hyatt, CJ, Haney-Caron, E, Stevens, MC (2011). Cortical thickness and folding deficits in conduct-disordered adolescents. Biological Psychiatry. Published online 29 December 2011. doi:10.1016/j.biopsych.2011.11.017.Google ScholarPubMed
Ishikawa, SS, Raine, A (2003). Prefrontal deficits and antisocial behavior: a causal model. In Causes of Conduct Disorder and Juvenile Delinquency (ed. Lahey, B. B., Moffitt, T. E. and Caspi, A.), pp. 277–304. Guilford Press: New York.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, 95–102.CrossRefGoogle ScholarPubMed
Jones, DK, Williams, SCR, Gasston, D, Horsfield, MA, Simmons, A, Howard, R (2002). Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time. Human Brain Mapping 15, 216–230.CrossRefGoogle Scholar
Kaufman, J, Birhamer, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, ND (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children – Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980–988.CrossRefGoogle ScholarPubMed
Kazdin, AE (1995). Conduct Disorders in Childhood and Adolescence. Sage: Thousand Oaks, CA.CrossRefGoogle Scholar
Kessler, RC, Nelson, CB, McGonagle, KA, Edlund, MJ, Frank, RG, Leaf, PJ (1996). The epidemiology of co-occurring addictive and mental disorders: implications for prevention and service utilization. American Journal of Orthopsychiatry 66, 17–31.CrossRefGoogle ScholarPubMed
Kiehl, KA, Smith, AM, Hare, RD, Mendrek, A, Forster, BB, Brink, J, Liddle, PF (2001). Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging. Biological Psychiatry 50, 677–684.CrossRefGoogle ScholarPubMed
Kruesi, MJ, Casanova, MF, Mannheim, G, Johnson-Bilder, A (2004). Reduced temporal lobe volume in early onset conduct disorder. Psychiatry Research 132, 1–11.CrossRefGoogle ScholarPubMed
Lebel, C, Walker, L, Leemans, A, Phillips, L, Beaulieu, C (2008). Microstructural maturation of the human brain from childhood to adulthood. NeuroImage 40, 1044–1055.CrossRefGoogle ScholarPubMed
Leemans, A, Jeurissen, B, Sijbers, J, Jones, DK (2009). ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Proceedings of the International Society for Magnetic Resonance in Medicine 17, 3537.Google Scholar
Levenston, GK, Patrick, CJ, Bradley, MM, Lang, PJ (2000). The psychopath as observer: emotion and attention in picture processing. Journal of Abnormal Psychology 109, 373–385.CrossRefGoogle ScholarPubMed
Li, Q, Sun, J, Guo, L, Zang, Y, Feng, Z, Huang, X, Yang, H, Huang, M, Gong, Q (2010). Increased fractional anisotropy in white matter of the right frontal region in children with attention-deficit/hyperactivity disorder: a diffusion tensor imaging study. Neuroendocrinology Letters 31, 747–753.Google ScholarPubMed
Marsh, AA, Finger, EC, Fowler, KA, Jurkowitz, IT, Schechter, JC, Yu, HH, Pine, DS, Blair, RJ (2011). Reduced amygdala-orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits. Psychiatry Research 194, 279–286.CrossRefGoogle ScholarPubMed
Marsh, AA, Finger, EC, Mitchell, DG, Reid, ME, Sims, C, Kosson, DS, Towbin, KE, Leibenluft, E, Pine, DS, Blair, RJ (2008). Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. American Journal of Psychiatry 165, 712–720.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Olsson, M (2009). DSM diagnosis of conduct disorder (CD) – a review. Nordic Journal of Psychiatry 63, 102–112.CrossRefGoogle ScholarPubMed
Pallant, J (2007). SPSS Survival Manual: A Step by Step Guide to Data Analysis using SPSS for Windows, 3rd edn.Open University Press: Maidenhead.Google Scholar
Paus, T (2010). Growth of white matter in the adolescent brain: myelin or axon? Brain and Cognition 72, 26–35.CrossRefGoogle ScholarPubMed
Raine, A, Buchsbaum, M, Lacasse, L (1997). Brain abnormalities in murderers indicated by positron emission tomography. Biological Psychiatry 42, 495–508.CrossRefGoogle ScholarPubMed
Raine, A, Lencz, T, Bihrle, S, LaCasse, L, Colletti, P (2000). Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Archives of General Psychiatry 57, 119–127.CrossRefGoogle ScholarPubMed
Sarkar, S, Clark, B, Deeley, Q (2011). Differences between psychopathy and other personality disorders: evidence from neuroimaging. Advances in Psychiatric Treatment 17, 191–200.CrossRefGoogle Scholar
Scholz, J, Klein, MC, Behrens, TEJ, Johansen-Berg, H (2009). Training induces changes in white-matter architecture. Nature Neuroscience 12, 1370–1371.CrossRefGoogle ScholarPubMed
Scott, S, Knapp, M, Henderson, J, Maughan, B (2001). Financial cost of social exclusion: follow up study of antisocial children into adulthood. British Medical Journal 323, 191–194.CrossRefGoogle ScholarPubMed
Scott, SK, Young, AW, Calder, AJ, Hellawell, DJ, Aggleton, JP, Johnson, M (1997). Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 385, 254–257.CrossRefGoogle ScholarPubMed
Silk, TJ, Vance, A, Rinehart, N, Bradshaw, JL, Cunnington, R (2009). White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Human Brain Mapping 30, 2757–2765.CrossRefGoogle ScholarPubMed
Smith, A, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TEJ, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Niazy, R, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 (S1), 208–219.CrossRefGoogle ScholarPubMed
Song, SK, Sun, SW, Ju, WK, Lin, SJ, Cross, AH, Neufeld, AH (2003). Diffusion tensor imaging detects and differentiates axonal and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 20, 1714–1722.CrossRefGoogle ScholarPubMed
Sterzer, P, Stadler, C (2009). Neuroimaging of aggressive and violent behaviour in children and adolescents. Frontiers in Behavioral Neuroscience 3, 1–8.CrossRefGoogle ScholarPubMed
Sterzer, P, Stadler, C, Poustka, F, Kleinschmidt, A (2007). A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. NeuroImage 37, 335–342.CrossRefGoogle ScholarPubMed
Sundram, F, Deeley, Q, Sarkar, S, Daly, E, Latham, R, Craig, MC, Fahy, F, Picchioni, M; UK AIMS Network, Barker, GJ, Murphy, DGM (2012). White matter microstructural abnormalities in the frontal lobe of adults with antisocial personality disorder. Cortex 48, 216–229.CrossRefGoogle ScholarPubMed
Versace, A, Almeida, JRC, Hassel, S, Walsh, ND, Novelli, M, Klein, CR, Kupfer, DJ, Phillips, ML (2008). Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Archives of General Psychiatry 65, 1041–1052.CrossRefGoogle ScholarPubMed
Vloet, TD, Konrad, K, Huebner, T, Herpertz, S, Herpertz-Dahlmann, B (2008). Structural and functional MRI-findings in children and adolescents with antisocial behavior. Behavioral Sciences and the Law 26, 99–111.CrossRefGoogle ScholarPubMed
Wang, R, Wedeen, VJ (2007). Diffusion Toolkit and TrackVis. Proceedings of the International Society for Magnetic Resonance in Medicine 15, 3720.Google Scholar
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. Pearson Education: San Antonio, TX.Google Scholar
Yang, Y, Raine, A, Narr, KL, Colletti, P, Toga, AW (2009). Localization of deformations within the amygdala in individuals with psychopathy. Archives of General Psychiatry 66, 986–994.CrossRefGoogle ScholarPubMed