Sex differences in neural responses to stress and alcohol context cues

Human Brain Mapping

Volumn 32, Issue 11, 2011, Pages 1998-2013

  Seo, Dongju ^a   Jia, Zhiru ^b   Lacadie, Cheryl M ^a   Tsou, Kristen A ^a   Bergquist, Keri ^a   Sinha, Rajita ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Alcohol cue; Brain fMRI; Prefrontal cortex; Reward; Sex differences; Stress

Indexed keywords

ALCOHOL;

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; CEREBELLUM; CLINICAL EXAMINATION; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DRINKING BEHAVIOR; EMOTIONAL STRESS; ENVIRONMENTAL STRESS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GUSTATORY CORTEX; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INTERPERSONAL STRESS; JOB STRESS; LIMBIC CORTEX; MALE; MENTAL DISEASE; MIDDLE FRONTAL GYRUS; NERVE POTENTIAL; NORMAL HUMAN; OCCIPITAL LOBE; ORBITAL CORTEX; PARIETAL LOBE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SEX DIFFERENCE; STRESS; VISUOMOTOR COORDINATION;

ADOLESCENT; ADULT; ALCOHOL DRINKING; ALCOHOLISM; AMYGDALA; ANXIETY; CEREBRAL CORTEX; CUES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGERY (PSYCHOTHERAPY); MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 80053621155     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21165     Document Type: Article

References (92)

1. Bagby RM, Taylor GJ, Parker JD (1988): Construct validity of the Toronto Alexithymia Scale. Psychother Psychosom 50: 29-34.
2. Barrett L, Lane R, Sechrest L, Schwartz G (2000): Sex differences in emotional awareness. Person Social Psychol Bull 26: 1027-1035.
3. Becker JB, Monteggia LM, Perrot-Sinal TS, Romeo RD, Taylor JR, Yehuda R, Bale TL (2007): Stress and disease: Is being female a predisposing factor? J Neurosci 27: 11851-11855.
4. Boscarino JA, Adams RE, Galea S (2006): Alcohol use in New York after the terrorist attacks: A study of the effects of psychological trauma on drinking behavior. Addict Behav 31: 606-621.
5. Brody LR, Hall J (1993): Gender and emotion. In: Lewis M, Haviland J, editors. Handbook of Emotions. N.Y.: Guilford Press. pp 447-460.
6. Cabeza R, Nyberg L (2000): Imaging cognition II: An empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12: 1-47.
7. Cacioppo JT, Gardner WL, Berntson GG (1999): The affect system has parallel and integrative processing components: Form follows function. J Person Social Psychol 76: 839-855.
8. Carver CS (2001): Affect and the functional bases of behavior: On the dimensional structure of affective experience. Person Social Psychol Rev 5: 345-356.
9. Chaplin TM, Hong K, Bergquist K, Sinha R (2008): Gender differences in response to emotional stress: An assessment across subjective, behavioral, and physiological domains and relations to alcohol craving. Alcohol Clin Exp Res 32: 1242-1250.
10. Chen EH, Dixon WJ (1972): Estimates of parameters of a censored regression sample. J Am Stat Assoc 67: 664-671.
11. Cohen S, Janicki-Deverts D, Miller GE (2007): Psychological stress and disease. JAMA 298: 1685-1687.
12. Cox RW (1996): AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29: 162-173.
13. Davidson RJ, Putnam KM, Larson CL (2000): Dysfunction in the neural circuitry of emotion regulation-A possible prelude to violence. Science 289: 591-594.
14. Dawson DA, Grant BF, Ruan WJ (2005): The association between stress and drinking: modifying effects of gender and vulnerability. Alcohol Alcohol 40: 453-460.
15. Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM, Sousa N (2009): Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325: 621-625.
16. Dixon WJ (1960): Simplified estimation from censored normal samples. Ann Math Stat 31: 385-391.
17. Duncan JS, Papademetris X, Yang J, Jackowski M, Zeng X, Staib LH (2004): Geometric strategies for neuroanatomic analysis from MRI. Neuroimage 23 (Suppl 1): S34-S45.
18. Epstein EE, Rhines KC, Cook S, Zdep-Mattocks B, Jensen NK, Mccrady BS (2006): Changes in alcohol craving and consumption by phase of menstrual cycle in alcohol dependent women. J Substance Use 11: 323-332.
19. Evans A, Collins D, Mills S, Brown E, Kelly R, Peters T (1993): 3D statistical neuroanatomical models from 305 MRI volumes. Proceedings of the Nuclear Science Symposium and Medical Imaging Conference, Vol. 3, San Francisco, CA, USA. pp 1813-1817.
20. Filbey FM, Claus E, Audette AR, Niculescu M, Banich MT, Tanabe J, Du YP, Hutchison KE (2008): Exposure to the taste of alcohol elicits activation of the mesocorticolimbic neurocircuitry. Neuropsychopharmacology 33: 1391-1401.
21. Fox HC, Hong KI, Siedlarz K, Sinha R (2008): Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine-dependent individuals compared to social drinkers. Neuropsychopharmacology 33: 796-805.
22. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996): Movement-related effects in fMRI time-series. Magn Reson Med 35: 346-355.
23. Garavan H, Pendergrass JC, Ross TJ, Stein EA, Risinger RC (2001): Amygdala response to both positively and negatively valenced stimuli. Neuroreport 12: 2779-2783.
24. George MS, Anton RF, Bloomer C, Teneback C, Drobes DJ, Lorberbaum JP, Nahas Z, Vincent DJ (2001): Activation of prefrontal cortex and anterior thalamus in alcoholic subjects on exposure to alcohol-specific cues. Arch Gen Psychiatry 58: 345-352.
25. Gilman JM, Ramchandani VA, Davis MB, Bjork JM, Hommer DW (2008): Why we like to drink: A functional magnetic resonance imaging study of the rewarding and anxiolytic effects of alcohol. J Neurosci 28: 4583-4591.
26. Goel V, Dolan RJ (2003): Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning. Neuroimage 20: 2314-2321.
27. Goldstein JM, Jerram M, Abbs B, Whitfield-Gabrieli S, Makris N (2010): Sex differences in stress response circuitry activation dependent on female hormonal cycle. J Neurosci 30: 431-438.
28. Grzywacz JG, Almeida DM (2008): Stress and binge drinking: A daily process examination of stressor pile-up and socioeconomic status in affect regulation. Int J Stress Manag 15: 364-380.
29. Haber SN, Knutson B (2010): The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology 35: 4-26.
30. Harris RE, Sundgren PC, Craig AD, Kirshenbaum E, Sen A, Napadow V, Clauw DJ (2009): Elevated insular glutamate in fibromyalgia is associated with experimental pain. Arthritis Rheum 60: 3146-3152.
31. 2 receptors in the ventral striatum and central processing of alcohol cues and craving. Am J Psychiatry 161: 1783-1789.
32. Herman RA, Wallen K (2007): Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure. Horm Behav 51: 496-507.
33. Hochberg Y (1988): A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75: 800-802.
34. Hollander JA, Lu Q, Cameron MD, Kamenecka TM, Kenny PJ (2008): Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105: 19480-19485.
35. Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC (1998): Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 22: 324-333.
36. Jackson ED, Payne JD, Nadel L, Jacobs WJ (2006): Stress differentially modulates fear conditioning in healthy men and women. Biol Psychiatry 59: 516-522.
37. Kahnt T, Park SQ, Cohen MX, Beck A, Heinz A, Wrase J (2009): Dorsal striatal-midbrain connectivity in humans predicts how reinforcements are used to guide decisions. J Cogn Neurosci 21: 1332-1345.
38. Kalbfleisch ML, Van Meter JW, Zeffiro TA (2007): The influences of task difficulty and response correctness on neural systems supporting fluid reasoning. Cogn Neurodyn 1: 71-84.
39. Karch S, Jager L, Karamatskos E, Graz C, Stammel A, Flatz W, Lutz J, Holtschmidt-Taschner B, Genius J, Leicht G, Pogarell O, Born C, Moller HJ, Hegerl U, Reiser M, Soyka M, Mulert C (2008): Influence of trait anxiety on inhibitory control in alcohol-dependent patients: Simultaneous acquisition of ERPs and BOLD responses. J Psychiatr Res 42: 734-745.
40. Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB (1993): Sex and depression in the National Comorbidity Survey. I. Lifetime prevalence, chronicity and recurrence. J Affect Disord 29: 85-96.
41. Kessler RC, McGonagle KA, Zhao S, Nelson CB, Hughes M, Eshleman S, Wittchen HU, Kendler KS (1994): Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 51: 8-19.
42. Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH (1999): Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 61: 154-162.
43. Koechlin E, Corrado G, Pietrini P, Grafman J (2000): Dissociating the role of the medial and lateral anterior prefrontal cortex in human planning. Proc Natl Acad Sci USA 97: 7651-7656.
44. Kraus T, Reulbach U, Bayerlein K, Mugele B, Hillemacher T, Sperling W, Kornhuber J, Bleich S (2004): Leptin is associated with craving in females with alcoholism. Addict Biol 9: 213-219.
45. Kudielka BM, Kirschbaum C (2005): Sex differences in HPA axis responses to stress: A review. Biol Psychol 69: 113-132.
46. Lang PJ. (2000): Emotion and motivation: Attention, perception, and action. J Sport Exercise Psychol 22: S122-S140.
47. Lang PJ, Bradley MM, Cuthbert MM. (1997): Motivated Attention: Affect, Activation and Action. Hillsdale, NJ: Lawrence Erlbaum Associates. 39 p.
48. Li CS, Kosten TR, Sinha R (2005): Sex differences in brain activation during stress imagery in abstinent cocaine users: A functional magnetic resonance imaging study. Biol Psychiatry 57: 487-494.
49. Li CS, Sinha R (2008): Inhibitory control and emotional stress regulation: Neuroimaging evidence for frontal-limbic dysfunction in psycho-stimulant addiction. Neurosci Biobehav Rev 32: 581-597.
50. Lindquist TL, Beilin LJ, Knuiman MW (1997): Influence of lifestyle, coping, and job stress on blood pressure in men and women. Hypertension 29( 1, Pt 1): 1-7.
51. Lopez JF, Akil H, Watson SJ (1999): Neural circuits mediating stress. Biol Psychiatry 46: 1461-1471.
52. Lukas SE, Mendelson JH, Benedikt RA, Jones B (1986): EEG alpha activity increases during transient episodes of ethanol-induced euphoria. Pharmacol Biochem Behav 25: 889-895.
53. MacDonald AW, III, Cohen JD, Stenger VA, Carter CS (2000): Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288: 1835-1838.
54. Modell JG, Mountz JM (1995): Focal cerebral blood flow change during craving for alcohol measured by SPECT. J Neuropsychiatry Clin Neurosci 7: 15-22.
55. Myrick H, Anton RF, Li X, Henderson S, Drobes D, Voronin K, George MS (2004): Differential brain activity in alcoholics and social drinkers to alcohol cues: Relationship to craving. Neuropsychopharmacology 29: 393-402.
56. Nachmias M, Gunnar M, Mangelsdorf S, Parritz RH, Buss K (1996): Behavioral inhibition and stress reactivity: The moderating role of attachment security. Child Dev 67: 508-522.
57. Nolen-Hoeksema S (1987): Sex differences in unipolar depression: Evidence and theory. Psychol Bull 101: 259-282.
58. Nolen-Hoeksema S, Larson J, Grayson C (1999): Explaining the gender difference in depressive symptoms. J Pers Soc Psychol 77: 1061-1072.
59. Nolf E, Voet T, Jacobs F, Dierckx R, Lemahieu I. (2003): XMedCon-An open-source medical image conversion toolkit. Eur J Nucl Med 30, S246.
60. Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JD, Gross JJ (2004): For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage 23: 483-499.
61. Office for National Statistics (2006): Smoking and drinking among adults. General Household Survey 2005.
62. Papademetris X (2006): BioImage Suite: An Intergrated Medical Image Analysis Suite [database on the Internet]. New Haven: Section of Bioimaging Sciences, Deptartment of Diagnostic Radiology, Yale School of Medicine.
63. Park SQ, Kahnt T, Beck A, Cohen MX, Dolan RJ, Wrase J, Heinz A (2010): Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci 30: 7749-7753.
64. Porrino LJ, Lyons D, Smith HR, Daunais JB, Nader MA (2004): Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J Neurosci 24: 3554-3562.
65. Roberts TA, Pennebaker JW (1995): Women's and men's strategies in perceiving internal state. In: Zanna IM, editor. Advances in Experimental Social Psychology. New York: Academic Press. pp 143-176.
66. Robinson TE, Berridge KC (1993): The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18: 247-291.
67. Rossi S, De Chiara V, Musella A, Mataluni G, Sacchetti L, Bernardi G, Usiello A, Centonze D (2009): Adaptations of striatal endocannabinoid system during stress. Mol Neurobiol 39: 178-184.
68. Rothemund Y, Preuschhof C, Bohner G, Bauknecht HC, Klingebiel R, Flor H, Klapp BF (2007): Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage 37: 410-421.
69. Rubonis AV, Colby SM, Monti PM, Rohsenow DJ, Gulliver SB, Sirota AD (1994): Alcohol cue reactivity and mood induction in male and female alcoholics. J Stud Alcohol 55: 487-494.
70. Sandstrom NJ (2007): Sex differences in use of visual cues by rhesus monkeys performing a spatial learning task: Comment on "Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure" by Herman and Wallen. Horm Behav 52: 139-142.
71. Sandstrom NJ, Kaufman J, Huettel SA (1998): Males and females use different distal cues in a virtual environment navigation task. Brain Res Cogn Brain Res 6: 351-360.
72. Schneider F, Habel U, Wagner M, Franke P, Salloum JB, Shah NJ, Toni I, Sulzbach C, Honig K, Maier W, Gaebel W, Zilles K (2001): Subcortical correlates of craving in recently abstinent alcoholic patients. Am J Psychiatry 158:1075-1083.
73. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, Seidenbecher CI, Coenen HH, Heinze HJ, Zilles K, Duzel E, Bauer A (2008): Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci 28: 14311-14319.
74. Sheehan P (1967): A shortened version of the Bett's questionnaire upon mental imagery. J Clin Psychol 23: 386-389.
75. Sinha R (2009a) Modeling stress and drug craving in the laboratory: Implications for addiction treatment development. Addict Biol 14: 84-98.
76. Sinha R. (2009b) Stress and addiction: A dynamic interplay of genes, environment, and drug intake. Biol Psychiatry 66: 100-101.
77. Sinha R, Fox HC, Hong KA, Bergquist K, Bhagwagar Z, Siedlarz KM (2009): Enhanced negative emotion and alcohol craving, and altered physiological responses following stress and cue exposure in alcohol dependent individuals. Neuropsychopharmacology 34: 1198-1208.
78. Sinha R, Garcia M, Paliwal P, Kreek MJ, Rounsaville BJ (2006): Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch Gen Psychiatry 63: 324-331.
79. Sinha R, Lacadie C, Skudlarski P, Wexler BE (2004): Neural circuits underlying emotional distress in humans. Ann NY Acad Sci 1032: 254-257.
80. Sinha R, Li CS (2007): Imaging stress- and cue-induced drug and alcohol craving: Association with relapse and clinical implications. Drug Alcohol Rev 26: 25-31.
81. Smith EE, Jonides J (1999): Storage and executive processes in the frontal lobes. Science 283: 1657-1661.
82. Tamres LK, Janicki D, Helgeson VS (2002): Sex differences in coping behavior: A meta-analytic review and an examination of relative coping. Person Social Psychol Rev 6: 2-30.
83. Vanderschuren LJ, Di Ciano P, Everitt BJ (2005): Involvement of the dorsal striatum in cue-controlled cocaine seeking. J Neurosci 25: 8665-8670.
84. Verona E, Reed A II, Curtin JJ, Pole M (2007): Gender differences in emotional and overt/covert aggressive responses to stress. Aggress Behav 33: 261-271.
85. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, Jayne M, Ma Y, Wong C (2006): Cocaine cues and dopamine in dorsal striatum: Mechanism of craving in cocaine addiction. J Neurosci 26: 6583-6588.
86. Willner P, Field M, Pitts K, Reeve G (1998): Mood, cue and gender influences on motivation, craving and liking for alcohol in recreational drinkers. Behav Pharmacol 9: 631-642.
87. Wilson SJ, Sayette MA, Fiez JA (2004): Prefrontal responses to drug cues: A neurocognitive analysis. Nat Neurosci 7: 211-214.
88. Wood GE, Beylin AV, Shors TJ (2001): The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav Neurosci 115: 175-187.
89. Wood GE, Shors TJ (1998): Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci USA 95: 4066-4071.
90. Wrase J, Schlagenhauf F, Kienast T, Wustenberg T, Bermpohl F, Kahnt T, Beck A, Strohle A, Juckel G, Knutson B, Heinz A (2007): Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage 35: 787-794.
91. Xiong J, Gao J-H, Lancaster JL, Fox PT (1995): Clustered pixels analysis for functional MRI activation studies of the human brain. Human Brain Mapp 3: 287-301.
92. Zhou Z, Zhu G, Hariri AR, Enoch MA, Scott D, Sinha R, Virkkunen M, Mash DC, Lipsky RH, Hu XZ, Hodgkinson CA, Xu K, Buzas B, Yuan Q, Shen PH, Ferrell RE, Manuck SB, Brown SM, Hauger RL, Stohler CS, Zubieta JK, Goldman D (2008): Genetic variation in human NPY expression affects stress response and emotion. Nature 452: 997-1001.