A selective insular perfusion deficit contributes to compromised salience network connectivity in recovering alcoholic men

Biological Psychiatry

Volumn 74, Issue 7, 2013, Pages 547-555

  Sullivan, Edith V ^a   Müller Oehring, Eva ^a,b   Pitel, Anne Lise ^a   Chanraud, Sandra ^a,b   Shankaranarayanan, Ajit ^c   Alsop, David C ^d   Rohlfing, Torsten ^b   Pfefferbaum, Adolf ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SRI INTERNATIONAL   (United States)

^c GE HEALTHCARE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Alcohol; arterial spin labeling; brain; connectivity; MRI; perfusion; working memory

Indexed keywords

ADULT; ALCOHOLISM; ANTERIOR CINGULATE; ARTERIAL SPIN LABELING; ARTICLE; BRAIN BLOOD FLOW; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DEFAULT MODE NETWORK; HUMAN; INSULA; MALE; MIDDLE FRONTAL GYRUS; PRECUNEUS; PRIORITY JOURNAL; REACTION TIME; REGIONAL PERFUSION; SPATIAL MEMORY; SPIN LABELING; WORKING MEMORY;

ALCOHOL; ARTERIAL SPIN LABELING; BRAIN; CONNECTIVITY; MRI; PERFUSION; WORKING MEMORY;

ALCOHOLISM; ATTENTION; BRAIN MAPPING; CEREBRAL CORTEX; HUMANS; MAGNETIC RESONANCE ANGIOGRAPHY; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; REST;

EID: 84883778858     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.02.026     Document Type: Article

References (90)

1. J.M. Nicolas, A.M. Catafau, R. Estruch, F.J. Lomena, M. Salamero, and R. Herranz Regional cerebral blood Flow-SPECT in chronic alcoholism: Relation to neuropsychological testing J Nucl Med 34 1993 1452 1459
2. A.C. Kuruoglu, Z. Arikan, G. Vural, M. Karatas, M. Arac, and E. Isik Single photon emission computerised tomography in chronic alcoholism. Antisocial personality disorder may be associated with decreased frontal perfusion Br J Psychiatry 169 1996 348 354
3. A. Tutus, N. Kugu, S. Sofuoglu, M. Nardali, A. Simsek, F. Karaaslan, and A.S. Gönül Transient frontal hypoperfusion in Tc-99m hexamethylpropyleneamineoxime single photon emission computed tomography imaging during alcohol withdrawal Biol Psychiatry 43 1998 923 928
4. D.A. Gansler, G.J. Harris, M. Oscar-Berman, C. Streeter, R.F. Lewis, I. Ahmed, and D. Achong Hypoperfusion of inferior frontal brain regions in abstinent alcoholics: A pilot SPECT study J Stud Alcohol 61 2000 32 37
5. D. Caspari, W. Trabert, G. Heinz, N. Lion, H. Henkes, and G. Huber The pattern of regional cerebral blood flow during alcohol withdrawal - a single photon emission tomography study with 99mTc-HMPAO Acta Psychiatr Scand 87 1993 414 417
6. M.S. George, C.C. Teneback, R.J. Malcolm, J. Moore, L.E. Stallings, and K.M. Spicer Multiple previous alcohol detoxifications are associated with decreased medial temporal and paralimbic function in the postwithdrawal period Alcohol Clin Exp Res 23 1999 1077 1084
7. Y. Suzuki, M. Oishi, K. Ogawa, and T. Mizutani Atrophy of the parahippocampal gyrus and regional cerebral blood flow in the limbic system in chronic alcoholic patients Alcohol 44 2010 439 445
8. G.P. Jordaan, J.M. Warwick, R. Hewlett, and R. Emsley Resting brain perfusion in alcohol-induced psychotic disorder: A comparison in patients with alcohol dependence, schizophrenia and healthy controls Prog Neuropsychopharmacol Biol Psychiatry 34 2010 479 485
9. G.J. Harris, M. Oscar-Berman, A. Gansler, C. Streeter, R.F. Lewis, I. Ahmed, and D. Achong Hypoperfusion of the cerebellum and aging effects on cerebral cortex blood flow in abstinent alcoholics: A SPECT study Alcohol Clin Exp Res 23 1999 1219 1227
10. B. Demir, B. Ulug, E. Lay Ergun, and B. Erbas Regional cerebral blood flow and neuropsychological functioning in early and late onset alcoholism Psychiatry Res 115 2002 115 125
11. B. Melgaard, L. Henriksen, P. Ahlgren, U.T. Danielsen, H. Sorensen, and O.B. Paulson Regional cerebral blood flow in chronic alcoholics measured by single photon emission computerized tomography Acta Neurol Scand 82 1990 87 93
12. A. Fellgiebel, A. Scheurich, T. Siessmeier, L.G. Schmidt, and P. Bartenstein Persistence of disturbed thalamic glucose metabolism in a case of Wernicke-Korsakoff syndrome Psychiatry Res 124 2003 105 112
13. D. Johnson-Greene, K.M. Adams, S. Gilman, K.J. Kluin, L. Junck, S. Martorello, and M. Heumann Impaired upper limb coordination in alcoholic cerebellar degeneration Arch Neurol 54 1997 436 439
14. T. Asada, S. Takaya, Y. Takayama, H. Yamauchi, K. Hashikawa, and H. Fukuyama Reversible alcohol-related dementia: A five-year follow-up study using FDG-PET and neuropsychological tests Intern Med 49 2010 283 287
15. G.J. Wang, N.D. Volkow, C.T. Roque, V.L. Cestaro, R.J. Hitzemann, and E.L. Cantos Functional importance of ventricular enlargement and cortical atrophy in healthy subjects and alcoholics as assessed with PET, MR imaging, and neuropsychologic testing Radiology 186 1993 59 65
16. K.M. Adams, S. Gilman, R.A. Koeppe, K.J. Kluin, J.A. Brunberg, and D. Dede Neuropsychological deficits are correlated with frontal hypometabolism in positron emission tomography studies of older alcoholic patients Alcohol Clin Exp Res 17 1993 205 210
17. 11C-glucose Acta Psychiatr Scand 78 1988 234 241
18. S. Gilman, K. Adams, R.A. Koeppe, S. Berent, K.J. Kluin, and J.G. Modell Cerebellar and frontal hypometabolism in alcoholic cerebellar degeneration studied with positron emission tomography Ann Neurol 28 1990 775 785
19. B. Biswal, F.Z. Yetkin, V.M. Haughton, and J.S. Hyde Functional connectivity in the motor cortex of resting human brain using echo-planar MRI Magn Reson Med 34 1995 537 541
20. D. Tomasi, and N.D. Volkow Association between functional connectivity hubs and brain networks Cereb Cortex 21 2011 2003 2013
21. C. Habas, N. Kamdar, D. Nguyen, K. Prater, C.F. Beckmann, V. Menon, and M.D. Greicius Distinct cerebellar contributions to intrinsic connectivity networks J Neurosci 29 2009 8586 8594
22. W.W. Seeley, V. Menon, A.F. Schatzberg, J. Keller, G.H. Glover, and H. Kenna Dissociable intrinsic connectivity networks for salience processing and executive control J Neurosci 27 2007 2349 2356
23. M. Raichle, A. MacLeod, A. Snyder, W. Powers, D. Gusnard, and G. Shulman A default mode of brain function Proc Natl Acad Sci U S A 98 2001 676 682
24. J.L. Vincent, A.Z. Snyder, M.D. Fox, B.J. Shannon, J.R. Andrews, M.E. Raichle, and R.L. Buckner Coherent spontaneous activity identifies a hippocampal-parietal memory network J Neurophysiol 96 2006 3517 3531
25. R.L. Buckner, J.R. Andrews-Hanna, and D.L. Schacter The brain's default network: Anatomy, function, and relevance to disease Ann N Y Acad Sci 1124 2008 1 38
26. M.D. Greicius, B. Krasnow, A.L. Reiss, and V. Menon Functional connectivity in the resting brain: A network analysis of the default mode hypothesis Proc Natl Acad Sci U S A 100 2003 253 258
27. M.D. Fox, A.Z. Snyder, J.L. Vincent, M. Corbetta, D.C. Van Essen, and M.E. Raichle The human brain is intrinsically organized into dynamic, anticorrelated functional networks Proc Natl Acad Sci U S A 102 2005 9673 9678
28. D. Sridharan, D.J. Levitin, and V. Menon A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks Proc Natl Acad Sci U S A 105 2008 12569 12574
29. M.E. Raichle, and D.A. Gusnard Intrinsic brain activity sets the stage for expression of motivated behavior J Comp Neurol 493 2005 167 176
30. G. Xu, H.A. Rowley, G. Wu, D.C. Alsop, A. Shankaranarayanan, and M. Dowling Reliability and precision of pseudo-continuous arterial spin labeling perfusion MRI on 3.0 T and comparison with 15O-water PET in elderly subjects at risk for Alzheimer's disease NMR Biomed 23 2010 286 293
31. F.Q. Ye, K.F. Berman, T. Ellmore, G. Esposito, J.D. van Horn, and Y. Yang H(2)(15)O PET validation of steady-state arterial spin tagging cerebral blood flow measurements in humans Magn Reson Med 44 2000 450 456
32. Raichle ME, Snyder AZ (2007): A default mode of brain function: A brief history of an evolving idea. Neuroimage 37:1083-1090; discussion 1097-1099.
33. J.A. Detre, J.S. Leigh, D.S. Williams, and A.P. Koretsky Perfusion imaging Magn Reson Med 23 1992 37 45
34. A. Pfefferbaum, S. Chanraud, A.-L. Pitel, E.M. Müller-Oehring, A. Shankaranarayanan, and D. Alsop Cerebral blood flow in posterior cortical nodes of the default mode network decreases with task engagement but remains higher than in most brain regions Cereb Cortex 21 2011 233 244
35. D.C. Alsop, W. Dai, M. Grossman, and J.A. Detre Arterial spin labeling blood flow MRI: Its role in the early characterization of Alzheimer's disease J Alzheimers Dis 20 2010 871 880
36. J. Wang, G.K. Aguirre, D.Y. Kimberg, A.C. Roc, L. Li, and J.A. Detre Arterial spin labeling perfusion fMRI with very low task frequency Magn Reson Med 49 2003 796 802
37. B.J. MacIntosh, K.T. Pattinson, D. Gallichan, I. Ahmad, K.L. Miller, and D.A. Feinberg Measuring the effects of remifentanil on cerebral blood flow and arterial arrival time using 3D GRASE MRI with pulsed arterial spin labelling J Cereb Blood Flow Metab 28 2008 1514 1522
38. G.K. Aguirre, J.A. Detre, E. Zarahn, and D.C. Alsop Experimental design and the relative sensitivity of BOLD and perfusion fMRI Neuroimage 15 2002 488 500
39. L.M. Parkes, W. Rashid, D.T. Chard, and P.S. Tofts Normal cerebral perfusion measurements using arterial spin labeling: Reproducibility, stability, and age and gender effects Magn Reson Med 51 2004 736 743
40. E.T. Petersen, K. Mouridsen, and X. Golay The QUASAR reproducibility study, Part II: Results from a multi-center Arterial Spin Labeling test-retest study Neuroimage 49 2010 104 113
41. A. Pfefferbaum, S. Chanraud, A.-L. Pitel, A. Shankaranarayanan, D.C. Alsop, T. Rohlfing, and E.V. Sullivan Volumetric cerebral perfusion imaging in healthy adults: Regional distribution, laterality, and repeatability of pulsed continuous arterial spin labeling (PCASL) Psychiatry Res 182 2010 266 273
42. T.F. Floyd, S.J. Ratcliffe, J. Wang, B. Resch, and J.A. Detre Precision of the CASL-perfusion MRI technique for the measurement of cerebral blood flow in whole brain and vascular territories J Magn Reson Imaging 18 2003 649 655
43. D.A. Gusnard, E. Akbudak, G.L. Shulman, and M.E. Raichle Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function Proc Natl Acad Sci U S A 98 2001 4259 4264
44. E.C. Wong, R.B. Buxton, and L.R. Frank A theoretical and experimental comparison of continuous and pulsed arterial spin labeling techniques for quantitative perfusion imaging Magn Reson Med 40 1998 348 355
45. R.B. Buxton, E.C. Wong, and L.R. Frank Dynamics of blood flow and oxygenation changes during brain activation: The balloon model Magn Reson Med 39 1998 855 864
46. J.A. Detre, J. Wang, Z. Wang, and H. Rao Arterial spin-labeled perfusion MRI in basic and clinical neuroscience Curr Opin Neurol 22 2009 348 355
47. W. Dai, D. Garcia, C. de Bazelaire, and D.C. Alsop Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields Magn Reson Med 60 2008 1488 1497
48. J. Camchong, A. Stenger, and G. Fein Resting-state synchrony during early alcohol abstinence can predict subsequent relapse [published online ahead of print July 20] Cereb Cortex. 2012
49. J. Camchong, A. Stenger, and G. Fein Resting-state synchrony in long-term abstinent alcoholics Alcohol Clin Exp Res 37 2013 75 85
50. A.L. Pitel, S. Chanraud, T. Rohlfing, A. Pfefferbaum, and E.V. Sullivan Face-name association learning and brain structural substrates in alcoholism Alcohol Clin Exp Res 36 2012 1171 1179
51. T. Schulte, E.M. Müller-Oehring, E.V. Sullivan, and A. Pfefferbaum Synchrony of corticostriatal-midbrain activation enables normal inhibitory control and conflict processing in recovering alcoholic men Biol Psychiatry 17 2012 269 278
52. E. Kim, J. Ku, K. Namkoong, W. Lee, K.S. Lee, and J.Y. Park Mammillothalamic functional connectivity and memory function in Wernicke's encephalopathy Brain 132 2009 369 376
53. O.G. O'Daly, L. Trick, J. Scaife, J. Marshall, D. Ball, and M.L. Phillips Withdrawal-associated increases and decreases in functional neural connectivity associated with altered emotional regulation in alcoholism Neuropsychopharmacology 37 2012 2267 2276
54. B.P. Rogers, M.H. Parks, M.K. Nickel, S.B. Katwal, and P.R. Martin Reduced fronto-cerebellar functional connectivity in chronic alcoholic patients Alcohol Clin Exp Res 36 2012 294 301
55. M.B. First, R.L. Spitzer, M. Gibbon, and J.B.W. Williams Structured Clinical Interview for DSM-IV Axis I Disorders (SCID) Version 2.0 1998 Biometrics Research Department, New York State Psychiatric Institute New York
56. H.F. Crovitz, and K.A. Zener Group test for assessing hand and eye dominance Am J Psychol 75 1962 271 276
57. A. Pfefferbaum, M.J. Rosenbloom, T. Rohlfing, E. Adalsteinsson, C.A. Kemper, S. Deresinski, and E.V. Sullivan Contribution of alcoholism to brain dysmorphology in HIV infection: Effects on the ventricles and corpus callosum Neuroimage 33 2006 239 251
58. H.A. Skinner Development and Validation of a Lifetime Alcohol Consumption Assessment Procedure 1982 Addiction Research Foundation Toronto
59. H.A. Skinner, and W.J. Sheu Reliability of alcohol use indices: The lifetime drinking history and the MAST J Stud Alcohol 43 1982 1157 1170
60. A. Pfefferbaum, K.O. Lim, R.B. Zipursky, D.H. Mathalon, M.J. Rosenbloom, and B. Lane Brain gray and white matter volume loss accelerates with aging in chronic alcoholics: A quantitative MRI study Alcohol Clin Exp Res 16 1992 1078 1089
61. W. Dai, P. Robson, A. Shankaranarayanan, and D.C. Alsop ASL perfusion measurement using a rapid, low resolution arterial transit time prescan In: Proceedings of the 17th International Society of Magnetic Resonance in Medicine, 2009 3585
62. S. Chanraud, A.L. Pitel, A. Pfefferbaum, and E.V. Sullivan Disruption of functional connectivity of the default-mode network in alcoholism Cereb Cortex 10 2011 2272 2281
63. T. Rohlfing, N.M. Zahr, E.V. Sullivan, and A. Pfefferbaum The SRI24 multichannel atlas of normal adult human brain structure Hum Brain Mapp 31 2010 798 819
64. S. Chanraud, A.-L. Pitel, T. Rohlfing, A. Pfefferbaum, and E.V. Sullivan Dual tasking and working memory in alcoholism: Relation to frontocerebellar circuitry Neuropsychopharmacology 35 2010 1868 1878
65. J.B. Poline, K.J. Worsley, A.C. Evans, and K.J. Friston Combining spatial extent and peak intensity to test for activations in functional imaging Neuroimage 5 1997 83 96
66. S. Chanraud, A.L. Pitel, E.M. Müller-Oehring, A. Pfefferbaum, and E.V. Sullivan Remapping the brain to compensate for impairment in recovering alcoholics Cereb Cortex 23 2013 97 104
67. D.S. Margulies, J.L. Vincent, C. Kelly, G. Lohmann, L.Q. Uddin, and B.B. Biswal Precuneus shares intrinsic functional architecture in humans and monkeys Proc Natl Acad Sci U S A 106 2009 20069 20074
68. S. Zhang, and C.S. Li Functional connectivity mapping of the human precuneus by resting state fMRI Neuroimage 59 2012 3548 3562
69. N. Khalili-Mahani, M.J. van Osch, E. Baerends, R.P. Soeter, M. de Kam, and R.W. Zoethout Pseudocontinuous arterial spin labeling reveals dissociable effects of morphine and alcohol on regional cerebral blood flow J Cereb Blood Flow Metab 31 2011 1321 1333
70. M.D. Greicius, K. Supekar, V. Menon, and R.F. Dougherty Resting-state functional connectivity reflects structural connectivity in the default mode network Cereb Cortex 19 2009 72 78
71. C.S. Li, X. Luo, P. Yan, K. Bergquist, and R. Sinha Altered impulse control in alcohol dependence: Neural measures of stop signal performance Alcohol Clin Exp Res 33 2009 740 750
72. E.B. Ansell, K. Rando, K. Tuit, J. Guarnaccia, and R. Sinha Cumulative adversity and smaller gray matter volume in medial prefrontal, anterior cingulate, and insula regions Biol Psychiatry 72 2012 57 64
73. M. Ullsperger, H.A. Harsay, J.R. Wessel, and K.R. Ridderinkhof Conscious perception of errors and its relation to the anterior insula Brain Struct Funct 214 2010 629 643
74. A.D. Craig How do you feel? Interoception: The sense of the physiological condition of the body Nat Rev Neurosci 3 2002 655 666
75. G.F. Koob, G. Kenneth Lloyd, and B.J. Mason Development of pharmacotherapies for drug addiction: A Rosetta stone approach Nat Rev Drug Discov 8 2009 500 515
76. G.F. Koob Neurobiological substrates for the dark side of compulsivity in addiction Neuropharmacology 56 suppl 1 2009 18 31
77. K.D. Ersche, A. Barnes, P.S. Jones, S. Morein-Zamir, T.W. Robbins, and E.T. Bullmore Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence Brain 134 2011 2013 2024
78. B. Adinoff, J. Braud, M.D. Devous, and T.S. Harris Caudolateral orbitofrontal regional cerebral blood flow is decreased in abstinent cocaine-addicted subjects in two separate cohorts Addict Biol 17 2011 1001 1012
79. N.H. Naqvi, and A. Bechara The insula and drug addiction: An interoceptive view of pleasure, urges, and decision-making Brain Struct Funct 214 2010 435 450
80. G.F. Koob, and N.D. Volkow Neurocircuitry of addiction Neuropsychopharmacology 35 2010 217 238
81. V. Menon, and L.Q. Uddin Saliency, switching, attention and control: A network model of insula function Brain Struct Funct 214 2010 655 667
82. C.P. Clark, G.G. Brown, L.T. Eyler, S.P. Drummond, D.R. Braun, and S.F. Tapert Decreased perfusion in young alcohol-dependent women as compared with age-matched controls Am J Drug Alcohol Abuse 33 2007 13 19
83. S. Gazdzinski, T. Durazzo, G.H. Jahng, F. Ezekiel, P. Banys, and D. Meyerhoff Effects of chronic alcohol dependence and chronic cigarette smoking on cerebral perfusion: A preliminary magnetic resonance study Alcohol Clin Exp Res 30 2006 947 958
84. A. Mon, T.C. Durazzo, S. Gazdzinski, and D.J. Meyerhoff The impact of chronic cigarette smoking on recovery from cortical gray matter perfusion deficits in alcohol dependence: Longitudinal arterial spin labeling MRI Alcohol Clin Exp Res 33 2009 1314 1321
85. G. Fein, V. Di Sclafani, and D. Meyerhoff Prefrontal cortical volume reduction associated with frontal cortex function deficit in 6-week abstinent crack-cocaine dependent men Drug Alcohol Depend 68 2002 87 93
86. J. O'Neill, V.A. Cardenas, and D.J. Meyerhoff Separate and interactive effects of cocaine and alcohol dependence on brain structures and metabolites: Quantitative MRI and proton MR spectroscopic imaging Addict Biol 6 2001 347 361
87. J.A. Matochik, E.D. London, D.A. Eldreth, J.L. Cadet, and K.I. Bolla Frontal cortical tissue composition in abstinent cocaine abusers: A magnetic resonance imaging study Neuroimage 19 2003 1095 1102
88. J. Tanabe, J.R. Tregellas, M. Dalwani, L. Thompson, E. Owens, T. Crowley, and M. Banich Medial orbitofrontal cortex gray matter is reduced in abstinent substance-dependent individuals Biol Psychiatry 65 2009 160 164
89. T.R. Franklin, P.D. Acton, J.A. Maldjian, J.D. Gray, J.R. Croft, and C.A. Dackis Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients Biol Psychiatry 51 2002 134 142
90. M.E. Raichle The restless brain Brain Connect 1 2011 3 12