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Sex-specific effects of cigarette smoking on caudate and amygdala volume and resting-state functional connectivity

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Abstract

Recent studies have demonstrated sex-specific differences in etiology, course and brain dysfunction that are associated with cigarette smoking. However, little is known about sex-specific differences in subcortical structure and function. In this study, structural and resting-state functional magnetic resonance imaging (fMRI) data were collected from 60 cigarette smokers (25 females) and 67 nonsmokers (28 females). The structural MRI was applied to identify deficits in sex-specific subcortical volume. Using resting-state fMRI, sex-related alterations in resting-state functional connectivity (rsFC) were investigated in subcortical nuclei with volume deficits as seed regions. Compared to nonsmokers, male but not female smokers demonstrated a significantly smaller volume in the left caudate, while female but not male smokers showed a smaller volume in the right amygdala. Resting-state FC analysis revealed that male but not female smokers had increased rsFC between the left caudate and the left prefrontal cortex but decreased rsFC within the bilateral caudate and between the right amygdala and right orbitofrontal cortex (OFC). Furthermore, the right amygdala volume was negatively correlated with the impulsivity score in female but not male smokers. The rsFC of the right amygdala-OFC circuit was negatively associated with the craving score in male but not female smokers. These findings indicate that cigarette smoking may have differential effects on the caudate and amygdala volumes as well as rsFC between men and women, contributing to our knowledge of sex-specific effects of nicotine addiction. Such sex-specific differences in subcortical structure and function may provide a methodological framework for the development of sex-specific relapse prevention therapies.

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References

  • Argyriou, E., Um, M., Carron, C., & Cyders, M. A. (2018). Age and impulsive behavior in drug addiction: A review of past research and future directions. Pharmacology Biochemistry and Behavior, 164, 106–117.

    CAS  Google Scholar 

  • Balevich, E. C., Wein, N. D., & Flory, J. D. (2013). Cigarette smoking and measures of impulsivity in a college sample. Substance Abuse, 34(3), 256–262.

    PubMed  PubMed Central  Google Scholar 

  • Barros-Loscertales, A., Garavan, H., Bustamante, J. C., Ventura-Campos, N., Llopis, J. J., Belloch, V., et al. (2011). Reduced striatal volume in cocaine-dependent patients. Neuroimage, 56(3), 1021–1026.

    CAS  PubMed  Google Scholar 

  • Bechara, A. (2005). Decision making, impulse control and loss of willpower to resist drugs: A neurocognitive perspective. Nature Neuroscience, 8(11), 1458–1463.

    CAS  PubMed  Google Scholar 

  • Becker, J. B., & Hu, M. (2008). Sex differences in drug abuse. Frontiers in Neuroendocrinology, 29(1), 36–47.

    CAS  PubMed  Google Scholar 

  • Beltz, A. M., Berenbaum, S. A., & Wilson, S. J. (2015). Sex differences in resting state brain function of cigarette smokers and links to nicotine dependence. Experimental and Clinical Psychopharmacology, 23(4), 247–254.

    PubMed  PubMed Central  Google Scholar 

  • Beylergil, S. B., Beck, A., Deserno, L., Lorenz, R. C., Rapp, M. A., Schlagenhauf, F., Heinz, A., & Obermayer, K. (2017). Dorsolateral prefrontal cortex contributes to the impaired behavioral adaptation in alcohol dependence. Neuroimage-Clinical, 15, 80–94.

    PubMed  PubMed Central  Google Scholar 

  • Birn, R. M., Molloy, E. K., Patriat, R., Parker, T., Meier, T. B., Kirk, G. R., Nair, V. A., Meyerand, M. E., & Prabhakaran, V. (2013). The effect of scan length on the reliability of resting-state fMRI connectivity estimates. Neuroimage, 83, 550–558.

    PubMed  PubMed Central  Google Scholar 

  • Britton, J. (2017). Death, disease, and tobacco. Lancet, 389(10082), 1861–1862.

    PubMed  Google Scholar 

  • Brody, A. L., Mandelkern, M. A., Jarvik, M. E., Lee, G. S., Smith, E. C., Huang, J. C., Bota, R. G., Bartzokis, G., & London, E. D. (2004). Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biological Psychiatry, 55(1), 77–84.

    PubMed  Google Scholar 

  • Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews Neuroscience, 7(6), 477–484.

    CAS  PubMed  Google Scholar 

  • Conti, A. A., McLean, L., Tolomeo, S., Steele, J. D., & Baldacchino, A. (2019). Chronic tobacco smoking and neuropsychological impairments: A systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews, 96, 143–154.

    CAS  PubMed  Google Scholar 

  • Contreras-Rodriguez, O., Albein-Urios, N., Vilar-Lopez, R., Perales, J. C., Martinez-Gonzalez, J. M., Fernandez-Serrano, M. J., et al. (2016). Increased corticolimbic connectivity in cocaine dependence versus pathological gambling is associated with drug severity and emotion-related impulsivity. Addiction Biology, 21(3), 709–718.

    CAS  PubMed  Google Scholar 

  • Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62(8), 847–855.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove, K. P., Wang, S., Kim, S. J., McGovern, E., Nabulsi, N., Gao, H., Labaree, D., Tagare, H. D., Sullivan, J. M., & Morris, E. D. (2014). Sex differences in the Brain's dopamine signature of cigarette smoking. Journal of Neuroscience, 34(50), 16851–16855.

    PubMed  Google Scholar 

  • Covey, L. S., Glassman, A. H., & Stetner, F. (1990). Depression and depressive symptoms in smoking cessation. Comprehensive Psychiatry, 31(4), 350–354.

    CAS  PubMed  Google Scholar 

  • Cox, L. S., Tiffany, S. T., & Christen, A. G. (2001). Evaluation of the brief questionnaire of smoking urges (QSU-brief) in laboratory and clinical settings. Nicotine & Tobacco Research, 3(1), 7–16.

    CAS  Google Scholar 

  • Crunelle, C. L., Kaag, A. M., van den Munkhof, H. E., Reneman, L., Homberg, J. R., Sabbe, B., et al. (2015). Dysfunctional amygdala activation and connectivity with the prefrontal cortex in current cocaine users. Human Brain Mapping, 36(10), 4222–4230.

    PubMed  PubMed Central  Google Scholar 

  • Das, D., Cherbuin, N., Anstey, K. J., Sachdev, P. S., & Easteal, S. (2012). Lifetime cigarette smoking is associated with striatal volume measures. Addiction Biology, 17(4), 817–825.

    CAS  PubMed  Google Scholar 

  • Dumais, K. M., Franklin, T. R., Jagannathan, K., Hager, N., Gawrysiak, M., Betts, J., Farmer, S., Guthier, E., Pater, H., Janes, A. C., & Wetherill, R. R. (2017). Multi-site exploration of sex differences in brain reactivity to smoking cues: Consensus across sites and methodologies. Drug and Alcohol Dependence, 178, 469–476.

    PubMed  PubMed Central  Google Scholar 

  • El Marroun, H., Schmidt, M. N., Franken, I. H. A., Jaddoe, V. W. V., Hofman, A., van der Lugt, A., et al. (2014). Prenatal tobacco exposure and brain morphology: A prospective study in Young children. Neuropsychopharmacology, 39(4), 792–800.

    PubMed  Google Scholar 

  • Faulkner, P., Petersen, N., Ghahremani, D. G., Cox, C. M., Tyndale, R. F., Hellemann, G. S., & London, E. D. (2018a). Sex differences in tobacco withdrawal and responses to smoking reduced-nicotine cigarettes in young smokers. Psychopharmacology, 235(1), 193–202.

    CAS  PubMed  Google Scholar 

  • Faulkner, P., Ghahremani, D. G., Tyndale, R. F., Paterson, N. E., Cox, C., Ginder, N., et al. (2018b). Neural basis of smoking-induced relief of craving and negative affect: Contribution of nicotine. Addiction Biology.

  • Feil, J., Sheppard, D., Fitzgerald, P. B., Yucel, M., Lubman, D. I., & Bradshaw, J. L. (2010). Addiction, compulsive drug seeking, and the role of frontostriatal mechanisms in regulating inhibitory control. Neuroscience and Biobehavioral Reviews, 35(2), 248–275.

    PubMed  Google Scholar 

  • Fields, S., Collins, C., Leraas, K., & Reynolds, B. (2009). Dimensions of impulsive behavior in adolescent smokers and nonsmokers. Experimental and Clinical Psychopharmacology, 17(5), 302–311.

    PubMed  PubMed Central  Google Scholar 

  • Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., & Dale, A. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.

    CAS  PubMed  Google Scholar 

  • Forray, A., Gilstad-Hayden, K., Suppies, C., Bogen, D., Sofuoglu, M., & Yonkers, K. A. (2017). Progesterone for smoking relapse prevention following delivery: A pilot, randomized, double-blind study. Psychoneuroendocrinology, 86, 96–103.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Franklin, T. R., Wetherill, R. R., Jagannathan, K., Johnson, B., Mumma, J., Hager, N., Rao, H., & Childress, A. R. (2014). The effects of chronic cigarette smoking on gray matter volume: Influence of sex. PLoS One, 9(8), e104102.

    PubMed  PubMed Central  Google Scholar 

  • Fritz, H. C., Wittfeld, K., Schmidt, C. O., Domin, M., Grabe, H. J., Hegenscheid, K., Hosten, N., & Lotze, M. (2014). Current smoking and reduced gray matter volume-a voxel-based Morphometry study. Neuropsychopharmacology, 39(11), 2594–2600.

    PubMed  PubMed Central  Google Scholar 

  • Gallinat, J., Meisenzahl, E., Jacobsen, L. K., Kalus, P., Bierbrauer, J., Kienast, T., Witthaus, H., Leopold, K., Seifert, F., Schubert, F., & Staedtgen, M. (2006). Smoking and structural brain deficits: A volumetric MR investigation. The European Journal of Neuroscience, 24(6), 1744–1750.

    PubMed  Google Scholar 

  • Goldstein, J. M., Seidman, L. J., Horton, N. J., Makris, N., Kennedy, D. N., Caviness, V. S., et al. (2001). Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex, 11(6), 490–497.

    CAS  PubMed  Google Scholar 

  • Goldstein, R. Z., & Volkow, N. D. (2002). Drug addiction and its underlying neurobiological basis: Neuroimaging evidence for the involvement of the frontal cortex. American Journal of Psychiatry, 159(10), 1642–1652.

    Google Scholar 

  • Gonzalez-Castillo, J., Handwerker, D. A., Robinson, M. E., Hoy, C. W., Buchanan, L. C., Saad, Z. S., et al. (2014). The spatial structure of resting state connectivity stability on the scale of minutes. Frontiers in Neuroscience, 8.

  • Greicius, M. D., Flores, B. H., Menon, V., Glover, G. H., Solvason, H. B., Kenna, H., Reiss, A. L., & Schatzberg, A. F. (2007). Resting-state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry, 62(5), 429–437.

    PubMed  PubMed Central  Google Scholar 

  • Gu, H., Salmeron, B. J., Ross, T. J., Geng, X. J., Zhan, W., Stein, E. A., et al. (2010). Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage, 53(2), 593–601.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hanlon, C. A., Owens, M. M., Joseph, J. E., Zhu, X., George, M. S., Brady, K. T., & Hartwell, K. J. (2016). Lower subcortical gray matter volume in both younger smokers and established smokers relative to non-smokers. Addiction Biology, 21(1), 185–195.

    PubMed  Google Scholar 

  • Heatherton, T. F., Kozlowski, L. T., Frecker, R. C., & Fagerstrom, K. O. (1991). The Fagerstrom test for nicotine dependence - a revision of the Fagerstrom tolerance questionnaire. British Journal of Addiction, 86(9), 1119–1127.

    CAS  PubMed  Google Scholar 

  • Kravitz, A. V., Tomasi, D., LeBlanc, K. H., Baler, R., Volkow, N. D., Bonci, A., et al. (2015). Cortico-striatal circuits: Novel therapeutic targets for substance use disorders. Brain Research, 1628, 186–198.

    CAS  PubMed  Google Scholar 

  • Kuhn, S., Romanowski, A., Schilling, C., Mobascher, A., Warbrick, T., Winterer, G., et al. (2012). Brain grey matter deficits in smokers: Focus on the cerebellum. Brain Structure & Function, 217(2), 517–522.

    Google Scholar 

  • Li, Y. D., Yuan, K., Cai, C. X., Feng, D., Yin, J. S., Bi, Y. Z., et al. (2015). Reduced frontal cortical thickness and increased caudate volume within fronto-striatal circuits in young adult smokers. Drug and Alcohol Dependence, 151, 211–219.

    PubMed  Google Scholar 

  • Liao, Y. H., Tang, J. S., Liu, T. Q., Chen, X. G., & Hao, W. (2012). Differences between smokers and non-smokers in regional gray matter volumes: A voxel-based morphometry study. Addiction Biology, 17(6), 977–980.

    PubMed  Google Scholar 

  • Lynch, W. J., & Sofuoglu, M. (2010). Role of progesterone in nicotine addiction: Evidence from initiation to relapse. Experimental and Clinical Psychopharmacology, 18(6), 451–461.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch, W. J., Roth, M. E., & Carroll, M. E. (2002). Biological basis of sex differences in drug abuse: Preclinical and clinical studies. Psychopharmacology, 164(2), 121–137.

    CAS  PubMed  Google Scholar 

  • McCarthy, J. M., Dumais, K. M., Zegel, M., Pizzagalli, D. A., Olson, D. P., Moran, L. V., et al. (2019). Sex differences in tobacco smokers: Executive control network and frontostriatal connectivity. Drug and Alcohol Dependence, 195, 59–65.

    PubMed  Google Scholar 

  • Melanko, S., Leraas, K., Collins, C., Fields, S., & Reynolds, B. (2009). Characteristics of psychopathy in adolescent nonsmokers and smokers: Relations to delay discounting and self reported impulsivity. Experimental and Clinical Psychopharmacology, 17(4), 258–265.

    PubMed  Google Scholar 

  • Mitchell, S. H. (1999). Measures of impulsivity in cigarette smokers and non-smokers. Psychopharmacology, 146(4), 455–464.

    CAS  PubMed  Google Scholar 

  • Mitchell, S. H. (2004). Measuring impulsivity and modeling its association with cigarette smoking. Behavioral and Cognitive Neuroscience Reviews, 3(4), 261–275.

    PubMed  Google Scholar 

  • Morales, A. M., Lee, B., Hellemann, G., O'Neill, J., & London, E. D. (2012). Gray-matter volume in methamphetamine dependence: Cigarette smoking and changes with abstinence from methamphetamine. Drug and Alcohol Dependence, 125(3), 230–238.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Lopez, L., Catena, A., Fernandez-Serrano, M. J., Delgado-Rico, E., Stamatakis, E. A., Perez-Garcia, M., et al. (2012). Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. Drug and Alcohol Dependence, 125(3), 208–214.

    PubMed  Google Scholar 

  • Narvacan, K., Treit, S., Camicioli, R., Martin, W., & Beaulieu, C. (2017). Evolution of deep gray matter volume across the human lifespan. Human Brain Mapping, 38(8), 3771–3790.

    PubMed  PubMed Central  Google Scholar 

  • Ng, M., Freeman, M. K., Fleming, T. D., Robinson, M., Dwyer-Lindgren, L., Thomson, B., Wollum, A., Sanman, E., Wulf, S., Lopez, A. D., Murray, C. J., & Gakidou, E. (2014). Smoking prevalence and cigarette consumption in 187 countries, 1980-2012. JAMA, 311(2), 183–192.

    CAS  PubMed  Google Scholar 

  • Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51(6), 768–774.

    CAS  PubMed  Google Scholar 

  • Peng, P., Wang, Z., Jiang, T., Chu, S., Wang, S., & Xiao, D. (2015). Brain-volume changes in young and middle-aged smokers: A DARTEL-based voxel-based morphometry study. Clin Respir J.

  • Perry, R. I., Krmpotich, T., Thompson, L. L., Mikulich-Gilbertson, S. K., Banich, M. T., & Tanabe, J. (2013). Sex modulates approach systems and impulsivity in substance dependence. Drug and Alcohol Dependence, 133(1), 222–227.

    PubMed  PubMed Central  Google Scholar 

  • Peters, S., Jolles, D. J., Van Duijvenvoorde, A. C. K., Crone, E. A., & Peper, J. S. (2015). The link between testosterone and amygdala-orbitofrontal cortex connectivity in adolescent alcohol use. Psychoneuroendocrinology, 53, 117–126.

    CAS  PubMed  Google Scholar 

  • Petersen, N., & London, E. D. (2018). Addiction and dopamine: Sex differences and insights from studies of smoking. Current Opinion in Behavioral Sciences, 23, 150–159.

    PubMed  PubMed Central  Google Scholar 

  • Pfefferbaum, A., Rosenbloom, M., Deshmukh, A., & Sullivan, E. V. (2001). Sex differences in the effects of alcohol on brain structure. American Journal of Psychiatry, 158(2), 188–197.

    CAS  Google Scholar 

  • Pomerleau, O. F., Pomerleau, C. S., Snedecor, S. M., Gaulrapp, S., Brouwer, R. N., & Cameron, O. G. (2004). Depression, smoking abstinence and HPA function in women smokers. Human Psychopharmacology-Clinical and Experimental, 19(7), 467–476.

    PubMed  Google Scholar 

  • Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59(3), 2142–2154.

    PubMed  Google Scholar 

  • Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2013). Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to carp. Neuroimage, 76(1), 439–441.

    PubMed  Google Scholar 

  • Rabinowicz, T., Dean, D. E., Petetot, J. M. C., & 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(2), 98–107.

    CAS  PubMed  Google Scholar 

  • Rando, K., Tuit, K., Hannestad, J., Guarnaccia, J., & Sinha, R. (2013). Sex differences in decreased limbic and cortical grey matter volume in cocaine dependence: A voxel-based morphometric study. Addiction Biology, 18(1), 147–160.

    PubMed  Google Scholar 

  • Resnick, S. M., Maki, P. M., Golski, S., Kraut, M. A., & Zonderman, A. B. (1998). Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Hormones and Behavior, 34(2), 171–182.

    CAS  PubMed  Google Scholar 

  • Reynolds, B., Patak, M., Shroff, P., Penfold, R. B., Melanko, S., & Duhig, A. M. (2007). Laboratory and self-report assessments of impulsive behavior in adolescent daily smokers and nonsmokers. Experimental and Clinical Psychopharmacology, 15(3), 264–271.

    PubMed  Google Scholar 

  • Romer, D. (2010). Adolescent risk taking, impulsivity, and brain development: Implications for prevention. Developmental Psychobiology, 52(3), 263–276.

    PubMed  PubMed Central  Google Scholar 

  • Ruigrok, A. N. V., Salimi-Khorshidi, G., Lai, M. C., Baron-Cohen, S., Lombardo, M. V., Tait, R. J., et al. (2014). A meta-analysis of sex differences in human brain structure. Neuroscience and Biobehavioral Reviews, 39, 34–50.

    PubMed  PubMed Central  Google Scholar 

  • Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., et al. (1998). The mini-international neuropsychiatric interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry, 59 Suppl 20, 22−33.

  • Shen, Z. J., Huang, P. Y., Wang, C., Qian, W., Luo, X., Guan, X. J., et al. (2017). Altered function but not structure of the amygdala in nicotine-dependent individuals. Neuropsychologia, 107, 102–107.

    PubMed  Google Scholar 

  • Sofuoglu, M., Babb, D. A., & Hatsukami, D. K. (2001). Progesterone treatment during the early follicular phase of the menstrual cycle: Effects on smoking behavior in women. Pharmacology Biochemistry and Behavior, 69(1–2), 299–304.

    CAS  Google Scholar 

  • Sofuoglu, M., Mitchell, E., & Mooney, M. (2009). Progesterone effects on subjective and physiological responses to intravenous nicotine in male and female smokers. Human Psychopharmacology-Clinical and Experimental, 24(7), 559–564.

    CAS  PubMed  Google Scholar 

  • Squeglia, L. M., Rinker, D. A., Bartsch, H., Castro, N., Chung, Y., Dale, A. M., Jernigan, T. L., & Tapert, S. F. (2014). Brain volume reductions in adolescent heavy drinkers. Developmental Cognitive Neuroscience, 9, 117–125.

    PubMed  PubMed Central  Google Scholar 

  • Streitburger, D. P., Moller, H. E., Tittgemeyer, M., Hund-Georgiadis, M., Schroeter, M. L., & Mueller, K. (2012). Investigating structural brain changes of dehydration using voxel-based Morphometry. PLoS One, 7(8).

  • Sullivan, E. V., Deshmukh, A., De Rosa, E., Rosenbloom, M. J., & Pfefferbaum, A. (2005). Striatal and forebrain nuclei volumes: Contribution to motor function and working memory deficits in alcoholism. Biological Psychiatry, 57(7), 768–776.

    PubMed  Google Scholar 

  • Tajima-Pozo, K., Ruiz-Manrique, G., Yus, M., Arrazola, J., & Montanes-Rada, F. (2015). Correlation between amygdala volume and impulsivity in adults with attention-deficit hyperactivity disorder. Acta Neuropsychiatrica, 27(6), 362–367.

    PubMed  Google Scholar 

  • Volkow, N. D., Fowler, J. S., & Wang, G. J. (2003). The addicted human brain: Insights from imaging studies. Journal of Clinical Investigation, 111(10), 1444–1451.

    CAS  PubMed Central  Google Scholar 

  • Weafer, J., & de Wit, H. (2014). Sex differences in impulsive action and impulsive choice. Addictive Behaviors, 39(11), 1573–1579.

    PubMed  Google Scholar 

  • Weiland, B. J., Sabbineni, A., Calhoun, V. D., Welsh, R. C., & Hutchison, K. E. (2015). Reduced executive and default network functional connectivity in cigarette smokers. Human Brain Mapping, 36(3), 872–882.

    PubMed  Google Scholar 

  • Wetherill, R. R., Jagannathan, K., Shin, J., & Franklin, T. R. (2014). Sex differences in resting state neural networks of nicotine-dependent cigarette smokers. Addictive Behaviors, 39(4), 789–792.

    PubMed  PubMed Central  Google Scholar 

  • Wetherill, R. R., Jagannathan, K., Hager, N., Maron, M., & Franklin, T. R. (2016). Influence of menstrual cycle phase on resting-state functional connectivity in naturally cycling, cigarette-dependent women. Biology of Sex Differences, 7.

  • Wetherill, R. R., Young, K. A., Jagannathan, K., Shin, J., O'Brien, C. P., Childress, A. R., et al. (2013). The impact of sex on brain responses to smoking cues: A perfusion fMRI study. Biology of Sex Differences, 4.

  • Wierenga, L. M., Bos, M. G. N., Schreuders, E., Vd Kamp, F., Peper, J. S., Tamnes, C. K., & Crone, E. A. (2018). Unraveling age, puberty and testosterone effects on subcortical brain development across adolescence. Psychoneuroendocrinology, 91, 105–114.

    CAS  PubMed  Google Scholar 

  • Woolley, C. S. (1999). Electrophysiological and cellular effects of estrogen on neuronal function. Critical Reviews in Neurobiology, 13(1), 1–20.

    CAS  PubMed  Google Scholar 

  • Yu, R., Zhao, L., & Lu, L. (2011). Regional grey and white matter changes in heavy male smokers. PLoS One, 6(11), e27440.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, S., Hu, S., Fucito, L. M., Luo, X. G., Mazure, C. M., Zaborszky, L., et al. (2017). Resting-state functional connectivity of the basal nucleus of Meynert in cigarette smokers: Dependence level and gender differences. Nicotine & Tobacco Research, 19(4), 452–459.

    Google Scholar 

  • Zhang, X. C., Salmeron, B. J., Ross, T. J., Geng, X. J., Yang, Y. H., & Stein, E. A. (2011). Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage, 54(1), 42–48.

    PubMed  Google Scholar 

  • Zung, W. W. (1965). A self-rating depression scale. Archives of General Psychiatry, 12, 63–70.

    CAS  PubMed  Google Scholar 

  • Zung, W. W. (1971). A rating instrument for anxiety disorders. Psychosomatics, 12(6), 371–379.

    CAS  PubMed  Google Scholar 

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Funding

This study was funded by the Natural Science Foundation of China (Nos. 81571757 and 81571650) and the Frontier Scientific Significant Breakthrough Project of CAS (No. QYZDB-SSW-SLH046).

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  1. National Center for Magnetic Resonance in Wuhan, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences, Wuhan, 430071, China

    Fuchun Lin & Hao Lei

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Fuchun Lin & Hao Lei

  3. Department of Radiology, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127, China

    Xu Han, Yao Wang, Weina Ding, Yawen Sun & Yan Zhou

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  1. Fuchun Lin
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Lin, F., Han, X., Wang, Y. et al. Sex-specific effects of cigarette smoking on caudate and amygdala volume and resting-state functional connectivity. Brain Imaging and Behavior 15, 1–13 (2021). https://doi.org/10.1007/s11682-019-00227-z

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