White matter microstructure alterations: A study of alcoholics with and without post-traumatic stress disorder

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Durkee, Caitlin A ^a   Sarlls, Joelle E ^b   Hommer, Daniel W ^a   Momenan, Reza ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALCOHOLISM; ANISOTROPY; BRAIN; BRAIN MAPPING; CASE CONTROL STUDY; COMPLICATION; DECISION MAKING; DIFFUSION TENSOR IMAGING; EMOTION; EXECUTIVE FUNCTION; FEMALE; HUMAN; IMAGE PROCESSING; MALE; MULTIVARIATE ANALYSIS; PATHOLOGY; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; STATISTICS AND NUMERICAL DATA;

ADULT; ALCOHOLISM; ANISOTROPY; BRAIN; BRAIN MAPPING; CASE-CONTROL STUDIES; DECISION MAKING; DIFFUSION TENSOR IMAGING; EMOTIONS; EXECUTIVE FUNCTION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MULTIVARIATE ANALYSIS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84894102678     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080952     Document Type: Article

References (75)

1. Fitzpatrick LE, Jackson M, Crowe SF (2008) The relationship between alcoholic cerebellar degeneration and cognitive and emotional functioning. Neurosci Biobehav Rev 32: 466-485. doi:10.1016/j.neubiorev.2007.08.004. PubMed: 17919727. (Pubitemid 351173330)
2. Hommer DW, Bjork JM, Gilman JM (2011) Imaging brain response to reward in addictive disorders. Ann N Y Acad Sci 1216: 50-61. doi: 10.1111/j.1749-6632. 2010.05898.x. PubMed: 21272010.
3. Stavro K, Pelletier J, Potvin S (2013) Widespread and sustained cognitive deficits in alcoholism: a meta-analysis. Addict Biol 18: 203-213. doi:10.1111/j.1369-1600.2011.00418.x. PubMed: 22264351.
4. Chanraud S, Martelli C, Delain F, Kostogianni N, Douaud G et al. (2007) Brain morphometry and cognitive performance in detoxified alcohol-dependents with preserved psychosocial functioning. Neuropsychopharmacology 32: 429-438. doi:10.1038/sj.npp.1301219. PubMed: 17047671. (Pubitemid 46106949)
5. Fein G, Di Sclafani V, Cardenas VA, Goldmann H, Tolou-Shams M et al. (2002) Cortical gray matter loss in treatment-naive alcohol dependent individuals. Alcohol Clin Exp Res 26: 558-564. doi: 10.1111/j.1530-0277.2002. tb02574.x. PubMed: 11981133. (Pubitemid 34408722)
6. Jernigan TL, Butters N, DiTraglia G, Schafer K, Smith T et al. (1991) Reduced cerebral grey matter observed in alcoholics using magnetic resonance imaging. Alcohol Clin Exp Res 15: 418-427. doi:10.1111/j.1530-0277.1991.tb00540. x. PubMed: 1877728.
7. Pfefferbaum A, Lim KO, Zipursky RB, Mathalon DH, Rosenbloom MJ et al. (1992) Brain gray and white matter volume loss accelerates with aging in chronic alcoholics: a quantitative MRI study. Alcohol Clin Exp Res 16: 1078-1089. doi:10.1111/j.1530-0277.1992.tb00702.x. PubMed: 1471762. (Pubitemid 23005150)
8. Agartz I, Shoaf S, Rawlings RR, Momenan R, Hommer DW (2003) CSF monoamine metabolites and MRI brain volumes in alcohol dependence. Psychiatry Res 122: 21-35. doi:10.1016/S0925-4927(02)00084-7. PubMed: 12589880. (Pubitemid 36183550)
9. Hommer D, Momenan R, Rawlings R, Ragan P, Williams W et al. (1996) Decreased corpus callosum size among alcoholic women. Arch Neurol 53: 359-363. doi:10.1001/archneur.1996.00550040099019. PubMed: 8929159. (Pubitemid 26110092)
10. Hommer D, Momenan R, Kaiser E, Rawlings R (2001) Evidence for a gender-related effect of alcoholism on brain volumes. Am J Psychiatry 158: 198-204. doi:10.1176/appi.ajp.158.2.198. PubMed: 11156801. (Pubitemid 32116516)
11. Pfefferbaum A, Rosenbloom MJ, Fama R, Sassoon SA, Sullivan EV (2010) Transcallosal white matter degradation detected with quantitative fiber tracking in alcoholic men and women: selective relations to dissociable functions. Alcohol Clin Exp Res 34: 1201-1211. PubMed: 20477772.
12. Bjork JM, Momenan R, Smith AR, Hommer DW (2008) Reduced posterior mesofrontal cortex activation by risky rewards in substance-dependent patients. Drug Alcohol Depend 95: 115-128. doi:10.1016/j.drugalcdep.2007.12.014. PubMed: 18295984.
13. Gilman JM, Davis MB, Hommer DW (2010) Greater activation in left hemisphere language-related regions during simple judgment tasks among substance-dependent patients in treatment for alcoholism. Alcohol Clin Exp Res 34: 331-341. doi:10.1111/j.1530-0277.2009.01095.x. PubMed: 19951293.
14. Salloum JB, Ramchandani VA, Bodurka J, Rawlings R, Momenan R et al. (2007) Blunted rostral anterior cingulate response during a simplified decoding task of negative emotional facial expressions in alcoholic patients. Alcohol Clin Exp Res 31: 1490-1504. doi:10.1111/j.1530-0277.2007.00447.x. PubMed: 17624997. (Pubitemid 47319655)
15. Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI. NeuroImage 73: 239-254. doi:10.1016/j.neuroimage.2012.06.081. PubMed: 22846632.
16. Chanraud S, Reynaud M, Wessa M, Penttilä J, Kostogianni N et al. (2009) Diffusion tensor tractography in mesencephalic bundles: relation to mental flexibility in detoxified alcohol-dependent subjects. Neuropsychopharmacology 34: 1223-1232. doi:10.1038/npp.2008.101. PubMed: 18615012.
17. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S et al. (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13: 534-546. doi:10.1002/jmri.1076. PubMed: 11276097. (Pubitemid 32231507)
18. Pfefferbaum A, Sullivan EV (2005) Disruption of brain white matter microstructure by excessive intracellular and extracellular fluid in alcoholism: evidence from diffusion tensor imaging. Neuropsychopharmacology 30(2): 423-432. doi:10.1038/sj.npp.1300623. PubMed: 15562292. (Pubitemid 40129494)
19. Harris GJ, Jaffin SK, Hodge SM, Kennedy D, Caviness VS et al. (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. PubMed: 18422840. (Pubitemid 351733083)
20. Pfefferbaum A, Rosenbloom M, Rohlfing T, Sullivan EV (2009) Degradation of association and projection white matter systems in alcoholism detected with quantitative fiber tracking. Biol Psychiatry 65: 680-690. doi:10.1016/j. biopsych.2008.10.039. PubMed: 19103436.
21. Pfefferbaum A, Sullivan EV, Hedehus M, Adalsteinsson E, Lim KO et al. (2000) In vivo detection and functional correlates of white matter microstructural disruption in chronic alcoholism. Alcohol Clin Exp Res 24: 1214-1221. doi:10.1111/j.1530-0277.2000.tb02086.x. PubMed: 10968660. (Pubitemid 30650940)
22. Pfefferbaum A, Sullivan EV (2002) Microstructural but not macrostructural disruption of white matter in women with chronic alcoholism. Neuroimage 15: 708-718. doi:10.1006/nimg.2001.1018. PubMed: 11848714. (Pubitemid 34852539)
23. Schulte T, Sullivan EV, Müller-Oehring EM, Adalsteinsson E, Pfefferbaum A (2005) Corpus callosal microstructural integrity influences interhemispheric processing: a diffusion tensor imaging study. Cereb Cortex 15: 1384-1392. PubMed: 15635059. (Pubitemid 41191545)
24. Yeh PH, Simpson K, Durazzo TC, Gazdzinski S, Meyerhoff DJ (2009) Tract-Based Spatial Statistics (TBSS) of diffusion tensor imaging data in alcohol dependence: abnormalities of the motivational neurocircuitry. Psychiatry Res 173: 22-30. doi:10.1016/j.pscychresns.2008.07.012. PubMed: 19442492.
25. Rosenbloom MJ, Sassoon SA, Fama R, Sullivan EV, Pfefferbaum A (2008) Frontal Callosal Fiber Integrity Selectively Predicts Coordinated Psychomotor Performance in Chronic Alcoholism. Brain Imaging Behav 2: 74-83. doi:10.1007/s11682-007-9017-9. PubMed: 19606265.
26. Pfefferbaum A, Sullivan EV (2002) Microstructural but not macrostructural disruption of white matter in women with chronic alcoholism. Neuroimage 15: 708-718. doi:10.1006/nimg.2001.1018. PubMed: 11848714. (Pubitemid 34852539)
27. Thomaes K, Dorrepaal E, Draijer N, de Ruiter MB, van Balkom AJ et al. (2010) Reduced anterior cingulate and orbitofrontal volumes in child abuse-related complex PTSD. J Clin Psychiatry 71: 1636-1644. doi: 10.4088/JCP.08m04754blu. PubMed: 20673548.
28. Bonne O, Brandes D, Gilboa A, Gomori JM, Shenton ME et al. (2001) Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. Am J Psychiatry 158: 1248-1251. doi:10.1176/appi.ajp.158.8.1248. PubMed: 11481158. (Pubitemid 32717698)
29. Lindauer RJ, Vlieger EJ, Jalink M, Olff M, Carlier IV et al. (2004) Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biol Psychiatry 56: 356-363. doi:10.1016/j.biopsych.2004.05.021. PubMed: 15336518. (Pubitemid 39164521)
30. Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35: 169-191. doi: 10.1038/npp.2009.83. PubMed: 19625997.
31. Bossini L, Tavanti M, Calossi S, Lombardelli A, Polizzotto NR et al. (2008) Magnetic resonance imaging volumes of the hippocampus in drug-naive patients with post-traumatic stress disorder without comorbidity conditions. J Psychiatr Res 42: 752-762. doi:10.1016/j.jpsychires.2007.08.004. PubMed: 17892884. (Pubitemid 351636102)
32. Abe O, Yamasue H, Kasai K, Yamada H, Aoki S et al. (2006) Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Res 146: 231-242. doi:10.1016/j.pscychresns.2006.01.004. PubMed: 16545552. (Pubitemid 43782727)
33. Kim MJ, Lyoo IK, Kim SJ, Sim M, Kim N et al. (2005) Disrupted white matter tract integrity of anterior cingulate in trauma survivors. Neuroreport 16: 1049-1053. doi:10.1097/00001756-200507130-00004. PubMed: 15973146. (Pubitemid 41017604)
34. Kim SJ, Jeong DU, Sim ME, Bae SC, Chung A et al. (2006) Asymmetrically altered integrity of cingulum bundle in posttraumatic stress disorder. Neuropsychobiology 54: 120-125. doi: 10.1159/000098262. PubMed: 17199097. (Pubitemid 46143895)
35. Schuff N, Zhang Y, Zhan W, Lenoci M, Ching C et al. (2011) Patterns of altered cortical perfusion and diminished subcortical integrity in posttraumatic stress disorder: an MRI study. NeuroImage 54 Suppl 1: S62-S68. doi:10.1016/j.neuroimage.2010.05.024. PubMed: 20483375.
36. Zhang L, Zhang Y, Li L, Li Z, Li W et al. (2011) Different white matter abnormalities between the first-episode, treatment-naive patients with posttraumatic stress disorder and generalized anxiety disorder without comorbid conditions. J Affect Disord 133: 294-299. doi:10.1016/j.jad.2011.03.040. PubMed: 21497403.
37. First MB, Spitzer RL, Gibbon M, Williams JBW (2002) User's Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders. Washington, DC: American Psychiatric Press, Inc.
38. Wechsler D (1981) Manual for the Wechsler Adult Intelligence Scale-Revised (WAIS-R). Psychological Corporation, New York.
39. Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence. New York, NY: The Psychological Corporation, Harcourt Brace & Company.
40. Pierpaoli C, Walker L, Irfanoglu MO, Barnett A, Basser P, et al. (2010) TORTOISE: an integrated software package for processing of diffusion MRI data, ISMRM 18th annual meeting, Stockholm, Sweden, #1597.
41. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE et al. (2006) Tract-based spatial statistics: voxelwise analysis of multisubject diffusion data. NeuroImage 31: 1487-1505. doi:10.1016/j.neuroimage.2006.02.024. PubMed: 16624579.
42. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 Suppl 1: S208-S219. doi: 10.1016/j.neuroimage.2004.07.051. PubMed: 15501092. (Pubitemid 39421720)
43. Aggleton JP, Neave N, Nagle S, Sahgal A (1995) A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions. J Neurosci 15: 7270-7281. PubMed: 7472481.
44. Schulte T, Mũller-Oehring EM, Pfefferbaum A, Sullivan EV (2010) Neurocircuitry of emotion and cognition in alcoholism: contributions from white matter fiber tractography. Dialogues Clin Neurosci 12: 554-560. PubMed: 21319499.
45. Sziklas V, Petrides M (1998) Memory and the region of the mammillary bodies. Prog Neurobiol 54: 55-70. doi:10.1016/S0301-0082(97)00064-6. PubMed: 9460793. (Pubitemid 28049819)
46. Vann SD, Aggleton JP (2004) The mammillary bodies: two memory systems in one? Nat Rev Neurosci 5: 35-44. doi:10.1038/nrn1299. PubMed: 14708002. (Pubitemid 38076182)
47. McQueeny T, Schweinsburg BC, Schweinsburg AD, Jacobus J, Bava S et al. (2009) Altered white matter integrity in adolescent binge drinkers. Alcohol Clin Exp Res 33: 1278-1285. doi:10.1111/j.1530-0277.2009.00953.x. PubMed: 19389185.
48. Jacobus J, Thayer RE, Trim RS, Bava S, Frank LR et al. (2012) White Matter Integrity, Substance Use, and Risk Taking in Adolescence. Psychol Addict Behav, 27: 431-42. PubMed: 22564204.
49. Grüsser SM, Wrase J, Klein S, Hermann D, Smolka MN et al. (2004) Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics. Psychopharmacology (Berl) 175: 296-302. doi:10.1007/s00213-004-1828-4. PubMed: 15127179. (Pubitemid 39361918)
50. Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30: 126-147. doi:10.1016/j.neubiorev.2005.06.006. PubMed: 16183121. (Pubitemid 41821805)
51. Myrick H, Anton RF, Li X, Henderson S, Drobes D et al. (2004) Differential brain activity in alcoholics and social drinkers to alcohol cues: relationship to craving. Neuropsychopharmacology 29: 393-402. doi:10.1038/sj.npp.1300295. PubMed: 14679386. (Pubitemid 38175156)
52. Hamner MB, Lorberbaum JP, George MS (1999) Potential role of the anterior cingulate cortex in PTSD: review and hypothesis. Depress Anxiety 9: 1-14. doi:10.1002/(SICI)1520-6394(1999)9:1. PubMed: 9989344. (Pubitemid 29061534)
53. Ito Y, Teicher MH, Glod CA, Harper D, Magnus E et al. (1993) Increased prevalence of electrophysiological abnormalities in children with psychological, physical, and sexual abuse. J Neuropsychiatry Clin Neurosci 5: 401-408. PubMed: 8286938. (Pubitemid 23326590)
54. Lanius RA, Williamson PC, Densmore M, Boksman K, Gupta MA et al. (2001) Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. Am J Psychiatry 158: 1920-1922. doi:10.1176/appi.ajp.158.11.1920. PubMed: 11691703. (Pubitemid 33054790)
55. Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML et al. (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47: 769-776. doi:10.1016/S0006-3223(00)00828-3. PubMed: 10812035. (Pubitemid 30254049)
56. Thiebaut de Schotten M, Dell'Acqua F, Valabregue R, Catani M (2012) Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48: 82-96. doi:10.1016/j.cortex.2011.10.001. PubMed: 22088488.
57. Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM et al. (2006) Top-down facilitation of visual recognition. Proc Natl Acad Sci U S A 103: 449-454. doi:10.1073/pnas.0507062103. PubMed: 16407167. (Pubitemid 43122421)
58. Tomita H, Ohbayashi M, Nakahara K, Hasegawa I, Miyashita Y (1999) Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401: 699-703. doi:10.1038/44372. PubMed: 10537108.
59. Baler RD, Volkow ND (2006) Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med 12: 559-566. doi:10.1016/j.molmed.2006.10.005. PubMed: 17070107. (Pubitemid 44780200)
60. Jacobus J, McQueeny T, Bava S, Schweinsburg BC, Frank LR et al. (2009) White matter integrity in adolescents with histories of marijuana use and binge drinking. Neurotoxicol Teratol 31: 349-355. doi:10.1016/j.ntt.2009.07.006. PubMed: 19631736.
61. Duncan JR, Dick AL, Egan G, Kolbe S, Gavrilescu M et al. (2012) Adolescent toluene inhalation in rats affects white matter maturation with the potential for recovery following abstinence. PLOS ONE 7: e44790. doi:10.1371/journal.pone.0044790. PubMed: 23028622.
62. Langlais PJ, Zhang SX (1997) Cortical and subcortical white matter damage without Wernicke's encephalopathy after recovery from thiamine deficiency in the rat. Alcohol Clin Exp Res 21: 434-443. doi: 10.1111/j.1530-0277.1997. tb03788.x. PubMed: 9161603. (Pubitemid 27217187)
63. Hoyumpa AM Jr. (1980) Mechanisms of thiamin deficiency in chronic alcoholism. Am J Clin Nutr 33: 2750-2761. PubMed: 6254354.
64. Saxena K, Tamm L, Walley A, Simmons A, Rollins N et al. (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. PubMed: 22375854.
65. Lent R, Schmidt SL (1993) The ontogenesis of the forebrain commissures and the determination of brain asymmetries. Prog Neurobiol 40: 249-276. doi:10.1016/0301-0082(93)90024-M. PubMed: 8430213.
66. Alhassoon OM, Sorg SF, Taylor MJ, Stephan RA, Schweinsburg BC et al. (2012) Callosal white matter microstructural recovery in abstinent alcoholics: a longitudinal diffusion tensor imaging study. Alcohol Clin Exp Res 36: 1922-1931. doi:10.1111/j.1530-0277.2012.01808.x. PubMed: 22551067.
67. Lebel C, Gee M, Camicioli R, Wieler M, Martin W et al. (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60: 340-352. doi:10.1016/j.neuroimage.2011.11.094. PubMed: 22178809.
68. Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD et al. (1995) The development of a Clinician-Administered PTSD Scale. J Trauma Stress 8: 75-90. doi:10.1002/jts.2490080106. PubMed: 7712061.
69. Bouzyk-Szutkiewicz J, Waszkiewicz N, Szulc A (2012) [Alcohol and psychiatric disorders]. Pol Merkur Lekarski 33: 176-181. PubMed: 23157139.
70. Regier DA, Farmer ME, Rae DS, Locke BZ, Keith SJ et al. (1990) Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epidemiologic Catchment Area (ECA) Study. JAMA 264: 2511-2518. doi:10.1001/jama.1990.03450190043026. PubMed: 2232018.
71. Enoch MA (2011) The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 214: 17-31. doi: 10.1007/s00213-010-1916-6. PubMed: 20596857.
72. Lovallo WR (2012) Early life adversity reduces stress reactivity and enhances impulsive behavior: Implications for health behaviors. Int J Psychophysiol. PubMed: 23085387
73. Bath KG, Schilit A, Lee FS (2013) Stress effects on BDNF expression: Effects of age, sex, and form of stress. Neuroscience, 239: 149-56. PubMed: 23402850.
74. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP (2002) Developmental neurobiology of childhood stress and trauma. Psychiatr Clin North Am 25: 397-426, vii-viii doi:10.1016/S0193-953X(01)00003-X. PubMed: 12136507.
75. Lauder JM (1983) Hormonal and humoral influences on brain development. Psychoneuroendocrinology 8: 121-155. doi: 10.1016/0306-4530(83)90053-7. PubMed: 6137852.