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

  • S. Sarkar (a1) (a2), M. C. Craig (a1) (a3) (a2), M. Catani (a1) (a3) (a2), F. Dell'Acqua (a1) (a3) (a2), T. Fahy (a1) (a3), Q. Deeley (a1) (a3) and D. G. M. Murphy (a1) (a3)...
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.

Copyright
Corresponding author
*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: sagari.sarkar@kcl.ac.uk)
References
Hide All
Adolphs, R, Tranel, D, Damasio, AR (1998). The human amygdala in social judgment. Nature 393, 470474.
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text revision (DSM-IV-TR). American Psychiatric Association: Washington, DC.
Basser, PJ, Pjevic, S, Pierpaoli, C, Duda, J, Aldoubi, A (2000). In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine 44, 625632.
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. 105126. Elsevier: London.
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, 11481150.
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.
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.
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, 491498.
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, 262276.
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, 720726.
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, 972981.
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, 552558.
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, 216220.
Catani, M, Howard, RJ, Pajevic, S, Jones, DK (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17, 7794.
Catani, M, Thiebaut de Schotten, M (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44, 11051132.
Chang, LC, Jones, DK, Pierpaoli, C (2005). RESTORE: robust estimation of tensors by outlier rejection. Magnetic Resonance in Medicine 53, 10881095.
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, 227234.
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, 233241.
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, 946953.
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, 280281.
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, 476477.
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, 843852.
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, 533539.
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, 12021213.
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, 20932100.
Fahim, C, He, Y, Yoon, U, Chen, J, Evans, AC, Perusse, D (2011). Neuroanatomy of childhood disruptive behavior disorders. Aggressive Behavior 37, 112.
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, 624633.
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, 586594.
Forth, AE, Kosson, D, Hare, RD (2003). Hare Psychopathy Checklist: Youth Version (PCL:YV). Multi-Health Systems Inc.: Toronto, Canada.
Frick, PJ (1998). Conduct Disorders and Severe Antisocial Behavior. Plenum: New York.
Frick, PJ, Hare, RD (2001). The Antisocial Process Screening Version (ASPD). Multi-Health Systems Inc.: Toronto, Canada.
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, 175185.
Gelhorn, HL, Sakai, JT, Price, RK, Crowley, TJ (2007). DSM-IV conduct disorder criteria as predictors of antisocial personality disorder. Comprehensive Psychiatry 48, 529538.
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, 779799.
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, 15241529.
Hare, RD (1991). The Hare Psychopathy Checklist – Revised, 1st edn.Multi-Health Systems, Inc.: Toronto, Ontario.
Horsfield, MA, Jones, DK (2002). Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR in Biomedicine 15, 570577.
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, 540547.
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.
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. 277304. Guilford Press: New York.
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, 95102.
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, 216230.
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, 980988.
Kazdin, AE (1995). Conduct Disorders in Childhood and Adolescence. Sage: Thousand Oaks, CA.
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, 1731.
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, 677684.
Kruesi, MJ, Casanova, MF, Mannheim, G, Johnson-Bilder, A (2004). Reduced temporal lobe volume in early onset conduct disorder. Psychiatry Research 132, 111.
Lebel, C, Walker, L, Leemans, A, Phillips, L, Beaulieu, C (2008). Microstructural maturation of the human brain from childhood to adulthood. NeuroImage 40, 10441055.
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.
Levenston, GK, Patrick, CJ, Bradley, MM, Lang, PJ (2000). The psychopath as observer: emotion and attention in picture processing. Journal of Abnormal Psychology 109, 373385.
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, 747753.
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, 279286.
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, 712720.
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.
Olsson, M (2009). DSM diagnosis of conduct disorder (CD) – a review. Nordic Journal of Psychiatry 63, 102112.
Pallant, J (2007). SPSS Survival Manual: A Step by Step Guide to Data Analysis using SPSS for Windows, 3rd edn.Open University Press: Maidenhead.
Paus, T (2010). Growth of white matter in the adolescent brain: myelin or axon? Brain and Cognition 72, 2635.
Raine, A, Buchsbaum, M, Lacasse, L (1997). Brain abnormalities in murderers indicated by positron emission tomography. Biological Psychiatry 42, 495508.
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, 119127.
Sarkar, S, Clark, B, Deeley, Q (2011). Differences between psychopathy and other personality disorders: evidence from neuroimaging. Advances in Psychiatric Treatment 17, 191200.
Scholz, J, Klein, MC, Behrens, TEJ, Johansen-Berg, H (2009). Training induces changes in white-matter architecture. Nature Neuroscience 12, 13701371.
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, 191194.
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, 254257.
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, 27572765.
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), 208219.
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, 17141722.
Sterzer, P, Stadler, C (2009). Neuroimaging of aggressive and violent behaviour in children and adolescents. Frontiers in Behavioral Neuroscience 3, 18.
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, 335342.
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, 216229.
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, 10411052.
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, 99111.
Wang, R, Wedeen, VJ (2007). Diffusion Toolkit and TrackVis. Proceedings of the International Society for Magnetic Resonance in Medicine 15, 3720.
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. Pearson Education: San Antonio, TX.
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, 986994.
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