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Association between functional brain alterations and neuropsychological scales in male chronic smokers using resting-state fMRI

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Abstract

Rationale

Recent studies have demonstrated that cigarette smoking is related to changes in brain structure and function. However, few studies focus on functional brain differences between male chronic smokers and nonsmokers in both local spontaneous activity and whole-brain functional networks.

Objectives

Our study recruited 67 chronic smokers and 43 nonsmokers who underwent functional magnetic resonance imaging (fMRI) scans to investigate functional activity and connectivity alterations in chronic smokers.

Methods

We used the mean fractional amplitude of the low-frequency fluctuation (mfALFF) and mean regional homogeneity (mReHo) methods to investigate resting-state spontaneous activity in chronic smokers and nonsmokers. The graph theoretical analysis (GTA) and network-based statistical (NBS) analysis were also used to investigate functional connectivity alterations.

Results

Compared with nonsmokers, chronic smokers exhibited higher activation in the reward system and portions of the prefrontal cortex but lower activation in the default mode networks (DMN) and visual-related regions. In addition, correlation analysis was conducted to assess the associations between neuroimaging findings and the severity of nicotine dependence or expectations of smoking effects. Our results showed that certain brain regions correlated with the Fagerström Test for Nicotine Dependence (FTND), the positive aspect of the Drug Use Disorders Identification Test Extended (DUDIT-E), and the negative aspect of the DUDIT-E, especially in the attentional control networks and hippocampus. The graph theoretical analysis (GTA) results indicated chronic smokers exhibited a trend toward increased assortativity. Our network-based statistical (NBS) analysis revealed reduced functional connections between the subnetwork in the prefrontal cortex, olfactory cortex, angular gyrus, and cingulate gyrus of chronic smokers.

Conclusions

We concluded that chronic smokers have neural adaptations in local spontaneous activity but remain healthy brain functional networks.

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References

  • Ambrose JA, Barua RS (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43:1731–1737

    Article  CAS  PubMed  Google Scholar 

  • Ayhan Z, Kaya M, Ozturk T, Karti O, Oner FH (2017) Evaluation of macular perfusion in healthy smokers by using optical coherence tomography angiography. Ophthalmic Surg Lasers Imaging Retina 48:617–622

    Article  PubMed  Google Scholar 

  • Baria AT, Baliki MN, Parrish T, Apkarian AV (2011) Anatomical and functional assemblies of brain BOLD oscillations. J Neurosci 31:7910–7919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12:512–523

    Article  PubMed  Google Scholar 

  • Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90–101

    Article  PubMed  Google Scholar 

  • Berkman ET, Falk EB, Lieberman MD (2011) In the trenches of real-world self-control: neural correlates of breaking the link between craving and smoking. Psychol Sci 22:498–506

    Article  PubMed  Google Scholar 

  • Brandon TH, Juliano LM, Copeland AL (1999) Expectancies for tobacco smoking. In: Kirsch I (ed) How expectancies shape experience. American Psychological Association, Washington, DC, pp 261–299

    Google Scholar 

  • Brody AL (2006) Functional brain imaging of tobacco use and dependence. J Psychiatr Res 40:404–418

    Article  PubMed  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349

    Article  CAS  PubMed  Google Scholar 

  • Claus ED, Blaine SK, Filbey FM, Mayer AR, Hutchison KE (2013) Association between nicotine dependence severity, BOLD response to smoking cues, and functional connectivity. Neuropsychopharmacology 38:2363–2372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  CAS  PubMed  Google Scholar 

  • Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. Am J Neuroradiol 22:1326–1333

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Paiva Fernandes TM, de Almeida NL, dos Santos NA (2017) Effects of smoking and smoking abstinence on spatial vision in chronic heavy smokers. Sci Rep 7:1–7

    CAS  Google Scholar 

  • Ding X, Yang Y, Stein EA, Ross TJ (2017) Combining multiple resting-state fMRI features during classification: optimized frameworks and their application to nicotine addiction. Front Hum Neurosci 11:362

    Article  PubMed  PubMed Central  Google Scholar 

  • Doll R, Peto R, Boreham J, Sutherland I (2004) Mortality in relation to smoking: 50 years’ observations on male British doctors. BMJ 328:1519

    Article  PubMed  PubMed Central  Google Scholar 

  • Due DL, Huettel SA, Hall WG, Rubin DC (2002) Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. Am J Psychiatry 159:954–960

    Article  PubMed  Google Scholar 

  • Durazzo TC, Meyerhoff DJ, Nixon SJ (2010) Chronic cigarette smoking: implications for neurocognition and brain neurobiology. Int J Environ Res Public Health 7:3760–3791

    Article  PubMed  PubMed Central  Google Scholar 

  • Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489

    Article  CAS  PubMed  Google Scholar 

  • Fedota JR, Stein EA (2015) Resting-state functional connectivity and nicotine addiction: prospects for biomarker development. Ann N Y Acad Sci 1349:64–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng D, Yuan K, Li Y, Cai C, Yin J, Bi Y, Cheng J, Guan Y, Shi S, Yu D (2016) Intra-regional and inter-regional abnormalities and cognitive control deficits in young adult smokers. Brain Imaging Behav 10:506–516

    Article  PubMed  Google Scholar 

  • Fritz H-C, Wittfeld K, Schmidt CO, Domin M, Grabe HJ, Hegenscheid K, Hosten N, Lotze M (2014) Current smoking and reduced gray matter volume—a voxel-based morphometry study. Neuropsychopharmacology 39:2594–2600

    Article  PubMed  PubMed Central  Google Scholar 

  • Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO (1991) The Fagerström test for nicotine dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86:1119–1127

    Article  CAS  PubMed  Google Scholar 

  • Henningfield JE, Miyasato K, Jasinski DR (1983) Cigarette smokers self-administer intravenous nicotine. Pharmacol Biochem Behav 19:887–890

    Article  CAS  PubMed  Google Scholar 

  • Hosseini SM, Hoeft F, Kesler SR (2012) GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS One 7:e40709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janes AC, Nickerson LD, Frederick BD, Kaufman MJ (2012) Prefrontal and limbic resting state brain network functional connectivity differs between nicotine-dependent smokers and non-smoking controls. Drug Alcohol Depend 125:252–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasinska AJ, Zorick T, Brody AL, Stein EA (2014) Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans. Neuropharmacology 84:111–122

    Article  CAS  PubMed  Google Scholar 

  • Katotomichelakis M, Balatsouras D, Tripsianis G, Davris S, Maroudias N, Danielides V, Simopoulos C (2007) The effect of smoking on the olfactory function. Rhinology 45:273

    PubMed  Google Scholar 

  • Kim J, Pignatelli M, Xu S, Itohara S, Tonegawa S (2016) Antagonistic negative and positive neurons of the basolateral amygdala. Nat Neurosci 19:1636–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Koob GF, Volkow ND (2016) Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry 3:760–773

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouimtsidis C, Stahl D, West R, Drummond C (2014) Can outcome expectancies be measured across substances? Development and validation of a questionnaire for populations in treatment. Drugs Alcohol Today 14:172–186

  • Lee J-H, Lim Y, Wiederhold BK, Graham SJ (2005) A functional magnetic resonance imaging (FMRI) study of cue-induced smoking craving in virtual environments. Appl Psychophysiol Biofeedback 30:195–204

    Article  PubMed  Google Scholar 

  • Lee K-H, Bowen S, An-Fu B (2011) Psychosocial outcomes of mindfulness-based relapse prevention in incarcerated substance abusers in Taiwan: a preliminary study. J Subst Abus 16:476–483

    Google Scholar 

  • Lin F, Wu G, Zhu L, Lei H (2015) Altered brain functional networks in heavy smokers. Addict Biol 20:809–819

    Article  PubMed  Google Scholar 

  • Malinowski P (2013) Neural mechanisms of attentional control in mindfulness meditation. Front Neurosci 7:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci 104:13170–13175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCarthy DM, Thompsen DM (2006) Implicit and explicit measures of alcohol and smoking cognitions. Psychol Addict Behav 20:436–444

    Article  PubMed  Google Scholar 

  • Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214:435–450

    Article  PubMed  PubMed Central  Google Scholar 

  • Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Organization WH (2019) WHO report on the global tobacco epidemic, 2019. World Health Organization, Geneva Google Scholar

    Google Scholar 

  • Pan P, Shi H, Zhong J, Xiao P, Shen Y, Wu L, Song Y, He G (2013) Chronic smoking and brain gray matter changes: evidence from meta-analysis of voxel-based morphometry studies. Neurol Sci 34:813–817

    Article  PubMed  Google Scholar 

  • Porrino LJ, Smith HR, Nader MA, Beveridge TJ (2007) The effects of cocaine: a shifting target over the course of addiction. Prog Neuro-Psychopharmacol Biol Psychiatry 31:1593–1600

    Article  CAS  Google Scholar 

  • Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci 98:676–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehme AK, Bey K, Frommann I, Mogg K, Bradley BP, Bludau J, Block V, Sträter B, Schütz CG, Wagner M (2018) Selective attention to smoking cues in former smokers. Eur Neuropsychopharmacol 28:276–284

    Article  CAS  PubMed  Google Scholar 

  • Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo X-N, Zhu C-Z, He Y, Yan C-G, Zang Y-F (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein EA, Pankiewicz J, Harsch HH, Cho J-K, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom AS (1998) Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatr 155:1009–1015

    Article  CAS  PubMed  Google Scholar 

  • Stoeckel LE, Chai XJ, Zhang J, Whitfield-Gabrieli S, Evins AE (2016) Lower gray matter density and functional connectivity in the anterior insula in smokers compared with never smokers. Addict Biol 21:972–981

    Article  PubMed  Google Scholar 

  • Sutherland MT, McHugh MJ, Pariyadath V, Stein EA (2012) Resting state functional connectivity in addiction: lessons learned and a road ahead. NeuroImage 62:2281–2295

    Article  PubMed  Google Scholar 

  • Sutherland MT, Riedel MC, Flannery JS, Yanes JA, Fox PT, Stein EA, Laird AR (2016) Chronic cigarette smoking is linked with structural alterations in brain regions showing acute nicotinic drug-induced functional modulations. Behav Brain Funct 12:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tanabe J, Nyberg E, Martin LF, Martin J, Cordes D, Kronberg E, Tregellas JR (2011) Nicotine effects on default mode network during resting state. Psychopharmacology 216:287–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanabe J, Regner M, Sakai J, Martinez D, Gowin J (2019) Neuroimaging reward, craving, learning, and cognitive control in substance use disorders: review and implications for treatment. Br J Radiol 92:20180942

    Article  PubMed  PubMed Central  Google Scholar 

  • Taniwaki T, Okayama A, Yoshiura T, Nakamura Y, Goto Y, J-i K, Tobimatsu S (2003) Reappraisal of the motor role of basal ganglia: a functional magnetic resonance image study. J Neurosci 23:3432–3438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Wang G-J, Telang F, Fowler JS, Logan J, Childress A-R, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Faith M, Patterson F, Tang K, Kerrin K, Wileyto EP, Detre JA, Lerman C (2007) Neural substrates of abstinence-induced cigarette cravings in chronic smokers. J Neurosci 27:14035–14040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins SS, Koob GF, Markou A (2000) Neural mechanisms underlying nicotine addiction: acute positive reinforcement and withdrawal. Nicotine Tob Res 2:19–37

    Article  CAS  PubMed  Google Scholar 

  • Wetter DW, Kenford SL, Welsch SK, Smith SS, Fouladi RT, Fiore MC, Baker TB (2004) Prevalence and predictors of transitions in smoking behavior among college students. Health Psychol 23:168–177

    Article  PubMed  Google Scholar 

  • Wilcox CE, Abbott CC, Calhoun VD (2019) Alterations in resting-state functional connectivity in substance use disorders and treatment implications. Prog Neuro-Psychopharmacol Biol Psychiatry 91:79–93

    Article  Google Scholar 

  • Wu G, Yang S, Zhu L, Lin F (2015) Altered spontaneous brain activity in heavy smokers revealed by regional homogeneity. Psychopharmacology 232:2481–2489

    Article  CAS  PubMed  Google Scholar 

  • Yu R, Zhao L, Tian J, Qin W, Wang W, Yuan K, Li Q, Lu L (2013) Regional homogeneity changes in heavy male smokers: a resting-state functional magnetic resonance imaging study. Addict Biol 18:729–731

    Article  PubMed  Google Scholar 

  • Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197–1207

    Article  PubMed  Google Scholar 

  • Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394–400

    Article  PubMed  Google Scholar 

  • Zhang X, Salmeron BJ, Ross TJ, Gu H, Geng X, Yang Y, Stein EA (2011) Anatomical differences and network characteristics underlying smoking cue reactivity. Neuroimage 54:131–141

    Article  PubMed  Google Scholar 

  • Zou Q-H, Zhu C-Z, Yang Y, Zuo X-N, Long X-Y, Cao Q-J, Wang Y-F, Zang Y-F (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172:137–141

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by the research program MOST105-2410-H-040-001-MY3 and MOST107-2221-E-182-054-MY3, which were sponsored by the Ministry of Science and Technology, Taipei, Taiwan. This study was also supported by grants NMRPD1H0101~3 of Chang Gung University, Taoyuan, Taiwan.

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Correspondence to Ming-Chou Ho.

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Weng, JC., Huang, SY., Lee, MS. et al. Association between functional brain alterations and neuropsychological scales in male chronic smokers using resting-state fMRI. Psychopharmacology 238, 1387–1399 (2021). https://doi.org/10.1007/s00213-021-05819-6

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