Top

Published in:

01-02-2016 | Original Article

Frontal white matter changes and aggression in methamphetamine dependence

Authors: Katharina Lederer, Jean-Paul Fouche, Don Wilson, Dan J. Stein, Anne Uhlmann

Published in: Metabolic Brain Disease | Issue 1/2016

Abstract

Chronic methamphetamine (MA) use can lead to white matter (WM) changes and increased levels of aggression. While previous studies have examined WM abnormalities relating to cognitive impairment, associations between WM integrity and aggression in MA dependence remain unclear. Diffusion Tensor Imaging (DTI) was used to investigate WM changes in 40 individuals with MA dependence and 40 matched healthy controls. A region of interest (ROI) approach using tract based spatial statistics (TBSS) in FSL was performed. We compared fractional anisotropy (FA), mean diffusivity (MD), parallel diffusivity (λ_║) and perpendicular diffusivity (λ_┴) in WM tracts of the frontal brain. A relationship of WM with aggression scores from the Buss & Perry Questionnaire was investigated. Mean scores for anger (p < 0.001), physical aggression (p = 0.032) and total aggression (p = 0.021) were significantly higher in the MA group relative to controls. ROI analysis showed increased MD (U = 439.5, p = 0.001) and λ_┴ (U = 561.5, p = 0.021) values in the genu of the corpus callosum, and increased MD (U = 541.5, p = 0.012) values in the right cingulum in MA dependence. None of the WM changes were significantly associated with aggression scores. This study provides evidence of frontal WM changes and increased levels of aggression in individuals with MA dependence. The lack of significant associations between WM and aggressive behaviour may reflect methodological issues in measuring such behaviour, or may indicate that the neurobiology of aggression is not simply correlated with WM damage but is more complex.

Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4:316–329. doi:10.1016/j.nurt.2007.05.011 PubMedPubMedCentralCrossRef

Alicata D, Chang L, Cloak C, Abe K, Ernst T (2009) Higher diffusion in striatum and lower fractional anisotropy in white matter of methamphetamine users. Psychiatry Res 174:1–8. doi:10.1016/j.pscychresns.2009.03.011 PubMedPubMedCentralCrossRef

Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15:435–455. doi:10.1002/nbm.782 PubMedCrossRef

Becker G (2007) The buss–Perry aggression questionnaire: some unfinished business. J Res Pers 41:434–452. doi:10.1016/j.jrp.2006.05.004 CrossRef

Bell RP, Foxe JJ, Nierenberg J, Hoptman MJ, Garavan H (2011) Assessing white matter integrity as a function of abstinence duration in former cocaine-dependent individuals. Drug Alcohol Depend 114:159–168. doi:10.1016/j.drugalcdep.2010.10.001 PubMedPubMedCentral

Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507. doi:10.1093/biomet/93.3.491 CrossRef

Beyer F, Münte TF, Wiechert J, Heldmann M, Krämer UM (2014) Trait aggressiveness is not related to structural connectivity between orbitofrontal cortex and amygdala. PLoS One 9:e101105. doi:10.1371/journal.pone.0101105 PubMedPubMedCentralCrossRef

Blumenfeld-Katzir T, Pasternak O, Dagan M, Assaf Y (2011) Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS One 6:e20678. doi:10.1371/journal.pone.0020678 PubMedPubMedCentralCrossRef

Boles SM, Miotto K (2003) Substance abuse and violence. Aggress Violent Behav 8:155–174. doi:10.1016/S1359-1789(01)00057-X CrossRef

Buss AH, Perry M (1992) The aggression questionnaire. J Pers Soc Psychol 63:452–459. doi:10.1037/0022-3514.63.3.452 PubMedCrossRef

Cadet JL, Krasnova IN, Jayanthi S, Lyles J (2007) Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotox Res 11:183–202. doi:10.1007/BF03033567 PubMedCrossRef

Cartier J, Farabee D, Prendergast ML (2006) Methamphetamine use, self-reported violent crime, and recidivism among offenders in California who abuse substances. J Interpersonal Violence 21:435–445. doi:10.1177/0886260505285724 CrossRef

Cercignani M, Inglese M, Pagani E, Comi G, FilippiI M (2001) Mean diffusivity and fractional anisotropy histograms of patients with multiple sclerosis. Am J neuroradiol 22:952–958 ISSN/ISBN0195-6108;0195-6108PubMed

Chermack ST, Walton MA, Fuller BE, Blow FC (2001) Correlates of expressed and received violence across relationship types among men and women substance abusers. Psychol Addict Behav 15:140–151. doi:10.1037/0893-164X.15.2.140 PubMedCrossRef

Coutlee CG, Huettel SA (2012) The functional neuroanatomy of decision making: prefrontal control of thought and action. Cogn Neurosci Thought 1428:3–12. doi:10.1016/j.brainres.2011.05.053

Craig MC, Catani M, Deeley Q, Latham R, Daly E, Kanaan R, Picchioni M, McGuire PK, Fahy T, Murphy DGM (2009) Altered connections on the road to psychopathy. Mol Psychiatry 14:946–953. doi:10.1038/mp.2009.40 PubMedCrossRef

Crowley TJ (1972) Dose-dependent facilitation or supression of rat fighting by methamphetamine, phenobarbital, or imipramine. Psychopharmacologia 27:213–222. doi:10.1007/BF00422801 PubMedCrossRef

Darke S (1998) Self-report among injecting drug users: a review. Drug Alcohol Depend 51:253–263 discussion 267–258PubMedCrossRef

Darke S, Kaye S, McKetin R, Duflou J (2008) Major physical and psychological harms of methamphetamine use. Drug Alcohol Rev 27:253–262. doi:10.1080/09595230801923702 PubMedCrossRef

Davidson RJ, Putnam KM, Larson CL (2000) Dysfunction in the neural circuitry of emotion regulation-a possible prelude to violence. Science (NY) 289:591–594. doi:10.1126/science.289.5479.591 CrossRef

Fals-Stewart W, Kashdan TB, O'Farrell TJ, Birchler GR (2002) Behavioral couples therapy for drug-abusing patients: effects on partner violence. J Subst Abus Treat 22:87–96. doi:10.1016/S0740-5472(01)00218-5 CrossRef

First MB, Spitzer RL, Gibbon M, Williams JBW (2002) Structured clinical interview for DSM-IV-TR axis I disorders, research version, non-patient edition (SCID-I/NP). New York State Psychiatric Institute Biometrics Research, New York

Geen RG (2001) Definition of aggression. In: Human aggression, vol 2nd. Open University Press, Buckingham, p 2

Goldman-Rakic PS, Selemon LD, Schwartz ML (1984) Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12:719–743. doi:10.1016/0306-4522(84)90166-0 PubMedCrossRef

Harris GJ, Jaffin SK, Hodge SM, Kennedy GJD, Caviness VS, Marinkovic K, Papadimitriou GM, Makris N, Oscar-Berman N (2008) Frontal white matter and cingulum diffusion tensor imaging deficits in alcoholism. Alcohol Clin Exp Res 32:1001–1013. doi:10.1111/j.1530-0277.2008.00661.x PubMedPubMedCentralCrossRef

Hasan KM, Alexander AL, Narayana PA (2004) Does fractional anisotropy have better noise immunity characteristics than relative anisotropy in diffusion tensor MRI? An analytical approach. Magn Reson Med 51:413–417. doi:10.1002/mrm.10682 PubMedCrossRef

Hoptman MJ, Volavka J, Johnson G, Weiss E, Bilder RM, Lim KO (2002) Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study. Biol Psychiatry 52:9–14. doi:10.1016/S0006-3223(02)01311-2 PubMedCrossRef

Huang W, DiFranza JR, Kennedy DN, Zhang N, Ziedonis D, Ursprung S, King JA (2013) Progressive levels of physical dependence to tobacco coincide with changes in the anterior cingulum bundle microstructure. PLoS One 8:e67837. doi:10.1371/journal.pone.0067837 PubMedPubMedCentralCrossRef

Kim IS, Kim YT, Song HJ, Lee JJ, Kwon DH, Lee HJ, Kim MN, Yoo DS, Chang Y (2009) Reduced corpus callosum white matter microstructural integrity revealed by diffusion tensor eigenvalues in abstinent methamphetamine addicts. Neurotoxicology 30:209–213. doi:10.1016/j.neuro.2008.12.002 PubMedCrossRef

Kim YT, Song HJ, Seo JH, Lee JJ, Lee J, Kwon DH, Yoo DS, Lee HJ, Suh KJ, Chang Y (2011) The differences in neural network activity between methamphetamine abusers and healthy subjects performing an emotion-matching task: functional MRI study. NMR Biomed 24:1392–1400. doi:10.1002/nbm.1702 PubMedCrossRef

Krasnova IN, Cadet JL (2009) Methamphetamine toxicity and messengers of death. Brain Res Rev 60:379–407. doi:10.1016/j.brainresrev.2009.03.002 PubMedPubMedCentralCrossRef

MacKinnon DP, Lockwood CM, Williams J (2004) Confidence limits for the indirect effect: distribution of the product and resampling methods. Multivar Behav Res 39:99. doi:10.1207/s15327906mbr3901_4 CrossRef

Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC (2001) Psychiatric aspects of impulsivity. Am J Psychiatr 158:1783–1793. doi:10.1176/appi.ajp.158.11.1783 PubMedCrossRef

Morgane PJ, Galler JR, Mokler DJ (2005) A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol 75:143–160. doi:10.1016/j.pneurobio.2005.01.001 PubMedCrossRef

Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga A, Pike B, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage 40:570–582. doi:10.1016/j.neuroimage.2007.12.035 PubMedPubMedCentralCrossRef

Nenonen M, Hakulinen U, Brander A, Ohman J, Dastidar P, Luoto TM (2015) Possible confounding factors on cerebral diffusion tensor imaging measurements. Acta Radiol Open 4(2):1–9. doi:10.1177/2047981614546795

Nowicka A, Tacokowski P (2011) Transcallosal transfer of information and functional asymmetry of the human brain. Laterality 16:35–74. doi:10.1080/13576500903154231 PubMed

Panenka WJ, Procyshyn RM, Lecomte T, MacEwan GW, Flynn SW, Honer WG, Barr AM (2013) Methamphetamine use: a comprehensive review of molecular, preclinical and clinical findings. Drug Alcohol Depend 129:167–179. doi:10.1016/j.drugalcdep.2012.11.016 PubMedCrossRef

Passamonti L, Fairchild G, Fornito A, Goodyer IM, Nimmo-Smith I, Hagan CC, Calder AJ (2012) Abnormal anatomical connectivity between the amygdala and orbitofrontal cortex in conduct disorder. PLoS One 7:e48789. doi:10.1371/journal.pone.0048789 PubMedPubMedCentralCrossRef

Payer DE, Lieberman MD, London ED (2011) Neural correlates of affect processing and aggression in methamphetamine dependence. Arch Gen Psychiatry 68:271–282. doi:10.1001/archgenpsychiatry.2010.154 PubMedPubMedCentralCrossRef

Peper JS, de Reus MA, van den Heuvel MP, Schutter DJLG (2014) Short fused? Associations between white matter connections, sex steroids, and aggression across adolescence. Hum Brain Mapp 36:1043–1052. doi:10.1002/hbm.22684 PubMedCrossRef

Plüddemann A, Flisher AJ, McKetin R, Parry C, Lombard C (2010) Methamphetamine use, aggressive behavior and other mental health issues among high-school students in Cape Town, South Africa. Drug Alcohol Depend 109:14–19. doi:10.1016/j.drugalcdep.2009.11.021 PubMedPubMedCentralCrossRef

Preacher KJ, Hayes AF (2004) SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behav Res Methods Instrum Comput 36:717–731. doi:10.3758/BF03206553 PubMedCrossRef

Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40:879–891. doi:10.3758/BRM.40.3.879 PubMedCrossRef

Ruesch N, Weber M, Il'Ysasov KA, Lieb K, Ebert D, Hennig J, Van Elst LT (2007) Inferior frontal white matter microstructure and patterns of psychopathology in women with borderline personality disorder and comorbid attention-deficit hyperactivity disorder. NeuroImage 35:738–747. doi:10.1016/j.neuroimage.2006.12.007 CrossRef

Salo R, Nordahl TE, Buonocore MH, Natsuaki Y, Waters C, Moore CD, Galloway GP, Leamon MH (2009) Cognitive control and white matter callosal microstructure in methamphetamine-dependent subjects: a diffusion tensor imaging study. Biol Psychiatry 65:122–128. doi:10.1016/j.biopsych.2008.08.004 PubMedPubMedCentralCrossRef

Saxena K, Tamm L, Walley A, Simmons A, Rollins N, Chia J, Soares JC, Emslie GJ, Fan X, Huang H (2012) A preliminary investigation of corpus callosum and anterior commissure aberrations in aggressive youth with bipolar disorders. J Child Adolesc Psychopharmacol 22:112–119. doi:10.1089/cap.2011.0063 PubMedPubMedCentralCrossRef

Schutter DJ, Harmon-Jones E (2013) The corpus callosum: a commissural road to anger and aggression. Neurosci Biobehav Rev 37:2481–2488. doi:10.1016/j.neubiorev.2013.07.013 PubMedCrossRef

Sekine Y, Ouchi Y, Takei N, Yoshikawa E, Nakamura K, Futatsubashi M, Okada H, Minabe Y, Suzuki K, Iwata Y, Tsuchiya KJ, Tsukada H, Iyo M, Mori N (2006) Brain serotonin transporter density and aggression in abstinent methamphetamine abusers. Arch Gen Psychiatry 63:90–100. doi:10.1001/archpsyc.63.1.90 PubMedCrossRef

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, Luca MD, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, Stefano ND, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23(Suppl 1):S208–S219PubMedCrossRef

Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TEJ (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31:1487–1505PubMedCrossRef

Sokolov BP, Schindler CW, Cadet JL (2004) Chronic methamphetamine increases fighting in mice. Pharmacol Biochem Behav 77:319–326. doi:10.1016/j.pbb.2003.11.006 PubMedCrossRef

Sommers I, Baskin D (2006) Methamphetamine use and violence. J Drug Issues 36:77–96. doi:10.1177/002204260603600104 CrossRef

Sommers I, Baskin D, Baskin-Sommers A (2006) Methamphetamine use among young adults: health and social consequences. Addict Behav 31:1469–1476. doi:10.1016/j.addbeh.2005.10.004 PubMedCrossRef

Sundram F, Deeley Q, Sarkar S, Daly E, Latham R, Craig M, Raczek M, Fahy T, Picchioni M, the UK AIMS Networkd, Barker GJ, Murphy DGM (2012) White matter microstructural abnormalities in the frontal lobe of adults with antisocial personality disorder. Cortex 48:216–229. doi:10.1016/j.cortex.2011.06.005 PubMedCrossRef

Tobias MC, O'Neill J, Hudkins M, Bartzokis G, Dean AC, London ED (2010) White-matter abnormalities in brain during early abstinence from methamphetamine abuse. Psychopharmacology 209:13–24. doi:10.1007/s00213-009-1761-7 PubMedPubMedCentralCrossRef

Walhovd KB, Johansen-Berg H, Káradóttir RT (2014) Unraveling the secrets of white matter – bridging the gap between cellular, animal and human imaging studies. Neuroscience 276:2–13. doi:10.1016/j.neuroscience.2014.06.05 PubMedPubMedCentralCrossRef

World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194. doi:10.1001/jama.2013.281053 CrossRef

Yamamoto BK, Moszczynska A, Gudelsky GA (2010) Amphetamine toxicities: classical and emerging mechanisms. Ann N Y Acad Sci 1187:101–121. doi:10.1111/j.1749-6632.2009.05141.x PubMedPubMedCentralCrossRef

Title: Frontal white matter changes and aggression in methamphetamine dependence
Authors: Katharina Lederer
Jean-Paul Fouche
Don Wilson
Dan J. Stein
Anne Uhlmann
Publication date: 01-02-2016
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 1/2016
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-015-9775-9

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Frontal white matter changes and aggression in methamphetamine dependence

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2016

Glutamatergic and HPA-axis pathway genes in bipolar disorder comorbid with alcohol- and substance use disorders

Neuropsychological manifestations in children with Sydenham’s chorea after adjunct intravenous immunoglobulin and standard treatment

Apolipoprotein E genotyping and questionnaire-based assessment of lifestyle risk factors in dyslipidemic patients with a family history of Alzheimer’s disease: test development for clinical application

A quantitative and qualitative review of the effects of testosterone on the function and structure of the human social-emotional brain

Genetic predisposition and early life experience interact to determine glutamate transporter (GLT1) and solute carrier family 12 member 5 (KCC2) levels in rat hippocampus

Memory deficits associated with khat (Catha edulis) use in rodents