Contributions of neuroimaging to understanding sex differences in cocaine abuse

Experimental and Clinical Psychopharmacology

Volumn 20, Issue 1, 2012, Pages 2-15

  Andersen, Monica L ^a,b   Sawyer, Eileen K ^a   Howell, Leonard L ^a,c  

^a EMORY UNIVERSITY   (United States)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal models; Cocaine; Drug abuse; MRI; Neuroimaging; PET; Sex differences; SPECT

Indexed keywords

AMPHETAMINE; COCAINE; DOPAMINE TRANSPORTER; ESTROGEN; PROGESTERONE; SEX HORMONE;

ARTICLE; BRAIN FUNCTION; COCAINE DEPENDENCE; DOPAMINE METABOLISM; DOPAMINERGIC SYSTEM; FEMALE; FOLLICULAR PHASE; HORMONE DETERMINATION; HUMAN; MALE; MENSTRUAL CYCLE; NEUROBIOLOGY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; SEX DIFFERENCE; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; ANIMAL; BLOOD; BRAIN; DRUG EFFECT; METHODOLOGY; PATHOPHYSIOLOGY; REVIEW; SEXUAL DEVELOPMENT;

ANIMALS; BRAIN; COCAINE-RELATED DISORDERS; FEMALE; GONADAL STEROID HORMONES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY; SEX CHARACTERISTICS; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 84860266025     PISSN: 10641297     EISSN: 19362293     Source Type: Journal    
DOI: 10.1037/a0025219     Document Type: Article

References (92)

1. Adinoff, B., Devous, M. D., Best, S. E., Harris, T. S., Chandler, P., Frock, S. D., & Williams, M. J. (2003). Regional cerebral blood flow in female cocaine-addicted subjects following limbic activation. Drug and Alcohol Dependence, 71, 255-268. doi:10.1016/S0376-8716(03)00138-8
2. Adinoff, B., Williams, M. J., Best, S. E., Harris, T. S., Chandler, P., & Devous, M. D., Sr. (2006). Sex differences in medial and lateral orbito- frontal cortex hypoperfusion in cocaine-dependent men and women. Gend. Med., 3, 206-222. doi:10.1016/S1550-8579(06)80209-3
3. Anker, J. J., Larson, E. B., Gliddonm, L. A., & Carroll, M. E. (2007). Effects of progesterone on the reinstatement of cocaine-seeking behavior in female rats. Experimental and Clinical Psychopharmacology, 15, 472-480. doi:10.1037/1064-1297.15.5.472
4. Aron, J. L. & Paulus, M. P. (2007). Location, location: Using functional magnetic resonance imaging to pinpoint brain differences relevant to stimulant use. Addiction, 102, 33-43. doi:10.1111/j.1360- 0443.2006.01778.x
5. Becker, J. B., & Hu, M. (2008). Sex differences in drug abuse. Frontiers in Neuroendocrinology, 29, 36-47. doi:10.1016/j.yfrne.2007.07.003
6. Becker, J. B., Molenda, H., & Hummer, D. L. (2001). Gender differ- ences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Annals of the New York Academy of Sciences, 937, 172-187. doi:10.1111/j.1749-6632.2001.tb03564.x
7. Best, S. E., Sarrel, P. M., Malison, R. T., Laruelle, M., Zoghbi, S. S., Baldwin, R. M., . . . van Dyck, C. H. (2005). Striatal dopamine trans- porter availability with [123I]beta-CIT SPECT is unrelated to gender or menstrual cycle. Psychopharmacology, 183, 181-189. doi:10.1007/ s00213-005-0158-5
8. Bowman, B. P., Vaughan, S. R., Walker, Q. D., Davis, S. L., Little, P. J., Scheffler, N. M., . . . Kuhn, C. M. (1999). Effects of sex and gonadec- tomy on cocaine metabolism in the rat. Journal of Pharmacology and Experimental Therapeutics, 290, 1316-1323.
9. Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Makris, N., Berke, J. D., . . . Hyman, S. E. (1997). Acute effects of cocaine on human brain activity and emotion. Neuron, 19, 591-611. doi:10.1016/ S0896-6273(00)80374-8
10. Castner, S. A., Xiao, L., & Becker, J. B. (1993). Sex differences in striatal dopamine: In vivo microdialysis and behavioral studies. Brain Research, 610, 127-134. doi:10.1016/0006-8993(93)91225-H
11. Chang, L., Ernst, T., Strickland, T., & Mehringer, C. M. (1999). Gender effects on persistent cerebral metabolite changes in the frontal lobes of abstinent cocaine users. American Journal of Psychiatry, 156, 716-722.
12. Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychia- try, 62, 847-855. doi:10.1016/j.biopsych.2007.03.001
13. Cotto, J. H., Davis, E., Dowling, G. J., Elcano, J. C., Staton, A. B., & Weiss, S. R. (2010). Gender effects on drug use, abuse, and dependence: A special analysis of results from the National Survey on Drug Use and Health. Gender Medicine, 7, 402-413.
14. Czoty, P. W., Riddick, N. V., Gage, H. D., Sandridge, M., Nader, S. H., Garg, S.,...Nader, M. A. (2009). Effect of menstrual cycle phase on dopamine D2 receptor availability in female cynomolgus monkeys. Neuropsychopharmacology, 34, 548-554.
15. DiChiara, G. (1995). The role of dopamine in drug abuse viewed from the perspective of its role in motivation. Drug and Alcohol Dependence, 38, 95-137. doi:10.1016/0376-8716(95)01118-I
16. Dluzen, D. E., & McDermott, J. L. (2006). Estrogen, testosterone, and methamphetamine toxicity. Annals of the New York Academy of Sci- ences, 1074, 282-294. doi:10.1196/annals.1369.025
17. Dreher, J. C., Schmidt, P. J., Kohn, P., Furman, D., Rubinow, D., & Berman, K. F. (2007). Menstrual cycle phase modulates reward-related neural function in women. Proc. Natl. Acad. Sci. USA, 104, 2465-2470. doi:10.1073/pnas.0605569104
18. Ernst, T., Chang, L., Oropilla, G., Gustavson, A., & Speck, O. (2000). Cerebral perfusion abnormalities in abstinent cocaine abusers: A perfu- sion MRI and SPECT study. Psychiatry Research, 99, 63-74. doi: 10.1016/S0925-4927(00)00056-1
19. Evans, S. M. (2007). The role of estradiol and progesterone in modulating the subjective effects of stimulants in humans. Experimental and Clin- ical Psychopharmacology, 15, 418-426. doi:10.1037/1064- 1297.15.5.418
20. Evans, S. M., & Foltin, R. W. (2006). Pharmacokinetics of repeated doses of intravenous cocaine across the menstrual cycle in rhesus monkeys. Pharmacology, Biochemistry and Behavior, 83, 56-66. doi:10.1016/ j.pbb.2005.12.007
21. Evans, S. M., & Foltin, R. W. (2010). Does the response to cocaine differ as a function of sex or hormonal status in human and non-human primates? Hormones and Behavior, 58, 13-21. doi:10.1016/j.yh- beh.2009.08.010
22. Evans, S. M., Haney, M., & Foltin, R. W. (2002). The effects of smoked cocaine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology, 159, 397-406. doi:10.1007/s00213-001- 0944-7
23. Farde, L., Hall., Pauli, S., & Halldin, C. (1995). Variability in D2- dopamine receptor density and affinity: A PET study with [11C] raclo- pride in man. Synapse, 20, 200-208. doi:10.1002/syn.890200303
24. Fattore, L., Altea, S., & Fratta, W. (2008). Sex differences in drug addic- tion: A review of animal and human studies. Women and Health, 4, 51-65. doi:10.2217/17455057.4.1.51
25. Febo, M., Ferris, C. F., & Segarra, A. C. (2005). Estrogen influences cocaine-induced blood oxygen level-dependent signal changes in female rats. Journal of Neuroscience, 25, 1132-1136. doi:10.1523/ JNEUROSCI.3801-04.2005
26. Fowler, J. S., Volkow, N. D., Kassed, C. A., & Chang, L. (2007). Imaging the addicted human brain. Sci. Pract. Perspect., 3, 4-16. doi:10.1151/ spp07324
27. Gardiner, S. A., Morrison, M. F., Mozley, P. D., Mozley, L. H., Brensinger, C., Bilker, W., . . . Battistini, M. (2004). Pilot study on the effect of estrogen replacement therapy on brain dopamine transporter availability in healthy, postmenopausal women. American Journal of Geriatric Psychiatry, 12, 621-630.
28. Gatley, S. J., Volkow, N. D., Wang, G. J., Fowler, J. S., Logan, J., Ding, Y. S., & Gerasimov, M. (2005). PET imaging in clinical drug abuse research. Curr. Pharm., 11, 3203-3219.
29. Goldstein, J. M., Jerram, M., Abbs, B., Whitfield-Gabrieli, S., & Makris, N. (2010). Sex differences in stress response circuitry activation depen- dent on female hormonal cycle. Journal of Neuroscience, 30, 431-438. doi:10.1523/JNEUROSCI.3021-09.2010
30. Hamilton, L. R., Czoty, P. W., Gage, H. D., & Nader, M. A. (2010). Characterization of the dopamine receptor system in adult rhesus mon- keys exposed to cocaine throughout gestation. Psychopharmacology, 210, 481-488. doi:10.1007/s00213-010-1847-2
31. Howell, L. L., & Murnane, K. S. (2008). Nonhuman primate neuroimaging and the neurobiology of psychostimulant addiction. Annals of the New York Academy of Sciences, 1141, 176-194. doi:10.1196/an- nals.1441.023
32. Howell, L. L., & Murnane, K. S. (2011). Nonhuman primate positron emission tomography neuroimaging in drug abuse research. Journal of Pharmacology and Experimental Therapeutics, 337, 324-334. doi: 10.1124/jpet.108.136689
33. Howell, L. L., & Wilcox, K. M. (2001). The dopamine transporter and cocaine medication development: Drug self-administration in nonhuman primates. Journal of Pharmacology and Experimental Therapeutics, 298, 1-6.
34. Hu, M., & Becker, J. B. (2003). Effects of sex and estrogen on behavioral sensitization to cocaine in rats. Journal of Neuroscience, 23, 693-699.
35. Hu, M., Crombag, H. S., Robinson, T. E., & Becker, J. B. (2004). Biological basis of sex differences in the propensity to self-administer cocaine. Neuropsychopharmacology, 29, 81-85. doi:10.1038/ sj.npp.1300301
36. Huettel, S. A., Song, A. W., & McCarty, G., Eds. (2003). Functional magnetic resonance imaging. Sunderland, MA: Sinauer Associates, Inc.
37. Justice, A. J. H., & de Wit, H. (1999). Acute effects of D-amphetamine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology, 145, 67-75. doi:10.1007/s002130051033
38. Kaasinen, V., Nagren, K., Hietala, J., Farde, L., & Rinne, J. O. (2001). Sex differences in extrastriatal dopamine D(2)-like receptors in the human brain. American Journal of Psychiatry, 158, 308-311. doi:10.1176/ appi.ajp.158.2.308
39. Kandel, D., Chen, K., Warner, L. A., Kessler, R. C., & Grant, B. (1997). Prevalence and demographic correlates of symptoms of last year depen- dence on alcohol, nicotine, marijuana and cocaine in the U.S. population. Drug and Alcohol Dependence, 44, 11-29. doi:10.1016/S0376- 8716(96)01315-4
40. Kaufman, M. J., Levin, J. M., Maas, L. C., Kukes, T. J., Villafuerte, R. A., Dostal, K., . . . Renshaw, P. F. (2001). Cocaine-induced cerebral vaso- constriction differs as a function of sex and menstrual cycle phase. Biological Psychiatry, 49, 774-781. doi:10.1016/S0006- 3223(00)01091-X
41. Kilts, C. D., Gross, R. E., Ely, T. D., & Drexler, K. P. (2004). The neural correlates of cue-induced craving in cocaine-dependent women. Amer- ican Journal of Psychiatry, 161, 233-241. doi:10.1176/ap- pi.ajp.161.2.233
42. Kosten, T., Gawin, F., Kosten, T., & Rounsaville, B. (1993). Gender differences in cocaine use and treatment response. Journal of Substance Abuse Treat, 10, 63-66. doi:10.1016/0740-5472(93)90100-G
43. Kuhn, C. M., Walker, Q. D., Kaplan, K. A., & Li, S. T. (2001). Sex, steroids, and stimulant sensitivity. Annals of the New York Academy of Sciences, 937, 188-201. doi:10.1111/j.1749-6632.2001.tb03565.x
44. Kuikka, J. T., Tiihonen, J., Karhu, J., Bergström, K. A., & Räsänen, P. (1997). Fractal analysis of striatal dopamine re-uptake sites. European Journal of Nuclear Medicine, 24, 1085-1090. doi:10.1007/BF01254238
45. Laruelle, M. (2000). Imaging synaptic neurotransmission with in vivo binding competition techniques: A critical review. Journal of Cerebral Blood Flow and Metabolism, 20, 423-451. doi:10.1097/00004647- 200003000-00001
46. Lavalaye, J., Booij, J., Reneman, L., Habraken, J. B., & van Royen, E. A. (2000). Effect of age and gender on dopamine transporter imaging with [123I]FP-CIT SPET in healthy volunteers. European Journal of Nuclear Medicine, 27, 867-869.
47. Levin, J. M., Holman, B. L., Mendelson, J. H., Teoh, S. K., Garada, B., Johnson, K. A., & Springer, S. (1994). Gender differences in cerebral perfusion in cocaine abuse: Technetium-99m-HMPAO SPECT study of drug-abusing women. Journal of Nuclear Medicine, 35, 1902-1909.
48. Li, C. S., Kosten, T. R., & Sinha, R. (2005). Sex differences in brain activation during stress imagery in abstinent cocaine users: A functional magnetic resonance imaging study. Biological Psychiatry, 57, 487-494. doi:10.1016/j.biopsych.2004.11.048
49. Lim, K. O., Wozniak, J. R., Mueller, B. A., Franc, D. T., Specker, S. M., Rodriguez, C. P., . . . Rotrosen, J. P. (2008). Brain macrostructural and microstructural abnormalities in cocaine dependence. Drug and Alcohol Dependence, 92, 164-172. doi:10.1016/j.drugalcdep.2007.07.019
50. Lynch, W. J., Roth, M. E., & Carroll, M. E. (2002). Biological basis of sex differences in drug abuse: Preclinical and clinical studies. Psychophar- macology, 164, 121-137. doi:10.1007/s00213-002-1183-2
51. Makris, N., Gasic, G. P., Seidman, L. J., Goldstein, J. M., Gastfriend, D. R., Elman, I., . . . Breiter, H. C. (2004). Decreased absolute amygdala volume in cocaine addicts. Neuron, 44, 729-740. doi:10.1016/ j.neuron.2004.10.027
52. Mash, D. C., Pablo, J., Ouyang, Q., Hearn, W. L., & Izenwasser, S. (2002). Dopamine transport function is elevated in cocaine users. Journal of Neurochemistry, 81, 292-300. doi:10.1046/j.1471-4159.2002.00820.x
53. McEwen, B. S., Alves, S. E., Bulloch, K., & Weiland, N. G. (1997). Ovarian steroids and the brain: Implications for cognition and aging. Neurology, 48, 8-15.
54. McEwen, B. S., & Parsons, B. (1982). Gonadal steroid action on the brain: Neurochemistry and neuropharmacology. Annual Review of Pharmacol- ogy and Toxicology, 22, 555-598. doi:10.1146/an- nurev.pa.22.040182.003011
55. Mello, N. K., Negus, S. S., Knudson, I. M., Kelly, M., & Mendelson, J. H. (2008). Effects of estradiol on cocaine self-administration and cocaine discrimination by female rhesus monkeys. Neuropsychopharmacology, 33, 783-795. doi:10.1038/sj.npp.1301451
56. Menzler, K., Belke, M., Wehrmann, E., Krakow, K., Lengler, U., Jansen, A., . . . Knake, S. (2011). Men and women are different: Diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thala- mus, corpus callosum and cingulum. Neuroimage, 54, 2557-2562. doi: 10.1016/j.neuroimage.2010.11.029
57. Minati, L., Grisoli, M., & Bruzzone, M. G. (2007). MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: A conceptual review. Journal of Geriatric Psychiatry and Neurology, 20, 3-21. doi:10.1177/0891988706297089
58. Mozley, L. H., Gur, R. C., Mozley, P. D., & Gur, R. E. (2001). Striatal dopamine transporters and cognitive functioning in healthy men and women. The American Journal of Psychiatry, 158, 1492-1499.
59. Munro, C. A., McCaul, M. E., Wong, D. F., Oswald, L. M., Zhou, Y., Brasic, J., . . . Wand, G. S. (2006). Sex differences in striatal dopamine release in healthy adults. Biological Psychiatry, 59, 966-974. doi: 10.1016/j.biopsych.2006.01.008
60. Nopoulos, P., Flaum, M., O'Leary, D., & Andreasen N. C. (2000). Sexual dimorphism in the human brain: Evaluation of tissue volume, tissue composition and surface anatomy using magnetic resonance imaging. Psychiatry Research, 98, 1-13. doi:10.1016/S0925-4927(99)00044-X
61. Nördstrom, A. L., Olsson, H., & Halldin, C. (1998). A PET study of D2 dopamine receptor density at different phases of the menstrual cycle. Psychiatry Research, 83, 1-6. doi:10.1016/S0925-4927(98)00021-3
62. Peris, J., Decambre, N., Coleman-Hardee, M., & Simpkins, J. (1991). Estradiol enhances behavioral sensitization to cocaine and amphetamine-stimulated [3H]dopamine release. Brain Research, 566, 255-264. doi:10.1016/0006-8993(91)91706-7
63. Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neuro- biology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54, 504-514. doi:10.1016/S0006- 3223(03)00168-9
64. Pletzer, B., Kronbichler, M., Aichhorn, M., Bergmann, J., Ladurner, G., & Kerschbaum, H. H. (2010). Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Research, 1348, 55-62. doi:10.1016/j.brainres.2010.06.019
65. Price, D. D. (2000). Psychological and neural mechanisms of the affective dimension of pain. Science, 288, 1769-1772. doi:10.1126/sci- ence.288.5472.1769
66. Protopopescu, X., Butler, T., Pan, H., Root, J., Altemus, M., Polanecsky, M., . . . Stern, E. (2008). Hippocampal structural changes across the menstrual cycle. Hippocampus, 18, 985-988. doi:10.1002/hipo.20468
67. Quiñones-Jenab, V., Perrotti, L. I., Fabian, S. J., Chin, J., Russo, S. J., & Jenab, S. (2001). Endocrinological basis of sex differences in cocaine- induced behavioral responses. Annals of the New York Academy of Sciences, 937, 140-171. doi:10.1111/j.1749-6632.2001.tb03563.x
68. Quinones-Jenab, V., Perrotti, L. I., Ho, A., Jenab, S., Schlussman, S. D., Franck, J., & Kreek, M. J. (2000). Cocaine affects progesterone plasma levels in female rats. Pharmacology, Biochemistry and Behavior, 66, 449-453. doi:10.1016/S0091-3057(00)00213-6
69. Rabinowicz, T., Dean, D. E., Petetot, J. M., & de Courten-Myers, G. M. (1999). Gender differences in the human cerebral cortex: More neurons in males; more processes in females. Journal of Child Neurology, 14, 98-107. doi:10.1177/088307389901400207
70. Raznahan, A., Lee, Y., Stidd, R., Long, R., Greenstein, D., Clasen, L., . . . Giedd, J. N. (2010). Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proc. Natl. Acad. Sci. USA, 107, 16988-16993. doi: 10.1073/pnas.1006025107
71. Riccardi, P., Zald, D., Li, R., Park, S., Ansari, M. S., Dawant, B., . . . Kessler, R. (2006). Sex differences in amphetamine-induced displace- ment of [(18)F]fallypride in striatal and extrastriatal regions: A PET study. American Journal of Psychiatry, 163, 1639-1641. doi:10.1176/ appi.ajp.163.9.1639
72. Robbins, S. J., Ehrman, R. N., Childress, A. R., & O'Brien, C. P. (1999). Comparing levels of cocaine cue reactivity in male and female outpa- tients. Drug and Alcohol Dependence, 53, 223-230. doi:10.1016/S0376- 8716(98)00135-5
73. Schlaepfer, T. E., Lancaster, E., Heidbreder, R., Strain, E. C., Kosel, M., Fisch, H. U., & Pearlson, G. D. (2006). Decreased frontal white-matter volume in chronic substance abuse. Int. J. Neuropsy- chopharmacol., 9, 147-153. doi:10.1017/S1461145705005705
74. Schwarz, A. J., Zocchi, A., Reese, T., Gozzi, A., Garzotti, M., Varnier, G., . . . Bifone, A. (2004). Concurrent pharmacological MRI and in situ microdialysis of cocaine reveal a complex relationship between the central hemodynamic response and local dopamine concentration. Neu- roimage, 23, 296-304. doi:10.1016/j.neuroimage.2004.05.001
75. Sell, S. L., Scalzitti, J. M., Thomas, M. L., & Cunningham, K. A. (2000). Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats. Journal of Pharmacology and Ex- perimental Therapeutics, 293, 879-886.
76. Senda, M., Kimura, Y., & Herscovitch, P. (Eds.). (2002). Brain imaging using PET. New York, NY: Academic Press.
77. Shin, Y. W., Kim, D. J., Ha, T. H., Park, H. J., Moon, W. J., Chung, E. C., . . . Kwon, J. S. (2005). Sex differences in the human corpus callosum: Diffusion tensor imaging study. Neuroreport, 16, 795-798. doi:10.1097/ 00001756-200505310-00003
78. Sofuoglu, M., Dudish-Poulsen, S., Nelson, D., Pentel, P. R., & Hatsukami, D. K. (1999). Sex and menstrual cycle differences in the subjective effects from smoked cocaine in humans. Experimental and Clinical Psychopharmacology, 7, 274-283. doi:10.1037/1064-1297.7.3.274
79. Substance Abuse and Mental Health Services Administration. (2010). Results from the 2009 National Survey on Drug Use and Health: Volume I. Summary of National Findings (Office of Applied Studies, NSDUH Series H-38A, HHS Publication No. SMA 10-4586 Findings). Rockville, MD.
80. Tomasi, D., Goldstein, R. Z., Telang, F., Maloney, T., Alia-Klein, N., Caparelli, E. C., & Volkow, N. D. (2007). Widespread disruption in brain activation patterns to a working memory task during cocaine abstinence. Brain Research, 1171, 83-92. doi:10.1016/ j.brainres.2007.06.102
81. Tucker, K. A., Browndyke, J. N., & Gottschalk, P. C. (2004). Gender- specific vulnerability for rCBF abnormalibities among cocaine abusers. Neuroreport, 15, 797-801. doi:10.1097/00001756-200404090-00011
82. van Dyck, C. H., Seibyl, J. P., Malison, R. T., Laruelle, M., Wallace, E., Zoghbi, S.S.,...Hoffer, P. B. (1995). Age-related decline in striatal dopamine trans- porter binding with iodine-123-beta-CIT SPECT. Journal of Nuclear Medicine, 36, 1175-1181.
83. Volkow, N. D., Fowler, J. S., Wang, G. J., Hitzemann, R., Logan, J., Schlyer, D. J., . . . Wolf, A. P. (1993). Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse, 14, 169-177. doi:10.1002/syn.890140210
84. Volkow, N. D., Fowler, J. S., Wolf, A. P., Schlyer, D., Shiue, C. Y., Alpert, R., . . . Henn, F. (1990). Effects of chronic cocaine abuse on postsynaptic dopamine receptors. American Journal of Psychiatry, 147, 719-724.
85. Volkow, N. D., Wang, G. J., Fowler, J. S., Logan, J., Gatley, S. J., Hitzemann, R., . . . Pappas, N. (1997). Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature, 386, 830-833. doi:10.1038/386830a0
86. Weiss, R., Martinez-Raga, J., Griffin, M., Greenfield, S., & Hufford, C. (1997). Gender differences in cocaine-dependent patients: A 6-month follow-up study. Drug and Alcohol Depend., 44, 35-40. doi:10.1016/ S0376-8716(96)01319-1
87. Witte, A. V., Savli, M., Holik, A., Kasper, S., & Lanzenberger, R. (2010). Regional sex differences in grey matter volume are associated with sex hormones in the young adult human brain. NeuroImage, 49, 1205-1212.
88. Wong, D. F., Broussolle, E. P., Wand, G., Villemagne, V., Dannals, R. F., Links, J. M., . . . Gjedde, A. (1988). In Vivo measurement of dopamine receptors in human brain by positron emission tomography: Age and sex differences. Annals of the New York Academy of Sciences, 515, 203-214. doi:10.1111/j.1749-6632.1988.tb32986.x
89. Wu, Q., Reith, M. E., Kuhar, M. J., Carroll, F. I., & Garris, P. A. (2001). Preferential increases in nucleus accumbens dopamine after systemic cocaine administration are caused by unique characteristics of dopamine neurotransmission. Journal of Neuroscience, 21, 6338-6347.
90. Xiao, Z., Lee, T., Zhang, J. X., Wu, Q., Wu, Rh, Weng, X., & Hu, X. (2006). Thirsty heroin show different fMRI activations when exposed to water-related and drug-related cues. Drug and Alcohol Depend., 83, 157-162. doi:10.1016/j.drugalcdep.2005.11.012
91. Xu, J., DeVito, E. E., Worhunsky, P. D., Carroll, K. M., Rounsaville, B. J., & Potenza, M. N. (2010). White matter integrity is associated with treatment outcome measures in cocaine dependence. Neuropsychophar- macology, 35, 1541-1549.
92. Yang, H., Zhao, W., Hu, M., & Becker, J. B. (2007). Interactions among ovarian hormones and time of testing on behavioral sensitization and cocaine self-administration. Behavioural Brain Research, 184, 174- 184. doi:10.1016/j.bbr.2007.07.005