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PLOS ONE  2014 

The Neural Mechanisms Underlying the Acute Effect of Cigarette Smoking on Chronic Smokers

DOI: 10.1371/journal.pone.0102828

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Abstract:

Although previous research had related structural changes and impaired cognition to chronic cigarette smoking, recent neuroimaging studies have associated nicotine, which is a main chemical substance in cigarettes, with improvements in cognitive functions (e.g. improved attention performance). However, information about the alterations of whole-brain functional connectivity after acute cigarette smoking is limited. In this study, 22 smokers underwent resting-state functional magnetic resonance imaging (rs-fMRI) after abstaining from smoking for 12 hours (state of abstinence, SOA). Subsequently, the smokers were allowed to smoke two cigarettes (state of satisfaction, SOS) before they underwent a second rs-fMRI. Twenty non-smokers were also recruited to undergo rs-fMRI. In addition, high-resolution 3D T1-weighted images were acquired using the same magnetic resonance imaging(fMRI)scanner for all participants. The results showed that smokers had structural changes in insula, thalamus, medial frontal cortex and several regions of the default mode network (DMN) compared with non-smokers. Voxel-wise group comparisons of newly developed global brain connectivity (GBC) showed that smokers in the SOA condition had higher GBC in the insula and superior frontal gyrus compared with non-smokers. However, smokers in the SOS condition demonstrated significantly lower GBC in several regions of the DMN, as compared with smokers in the SOA condition. These results suggest that structural integrity combined with dysfunction of the DMN might be involved in relapses after a short period of time among smokers.

References

[1]  Warner K, MacKay J (2006) The global tobacco disease pandemic: nature, causes, and cures. Global public health 1: 65–86. doi: 10.1080/17441690500430771
[2]  Yang G, Kong L, Zhao W, Wan X, Zhai Y, et al. (2008) Emergence of chronic non-communicable diseases in China. The Lancet 372: 1697–1705. doi: 10.1016/s0140-6736(08)61366-5
[3]  West R, Shiffman S (2007) Fast facts: smoking cessation: Health Press Limited.
[4]  Liao Y, Tang J, Liu T, Chen X, Hao W (2010) Differences between smokers and non-smokers in regional gray matter volumes: a voxel-based morphometry study. Addiction Biology.
[5]  Brody AL, Mandelkern MA, Jarvik ME, Lee GS, Smith EC, et al. (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biological psychiatry 55: 77–84. doi: 10.1016/s0006-3223(03)00610-3
[6]  Gallinat J, Meisenzahl E, Jacobsen LK, Kalus P, Bierbrauer J, et al. (2006) Smoking and structural brain deficits: a volumetric MR investigation. European Journal of Neuroscience 24: 1744–1750. doi: 10.1111/j.1460-9568.2006.05050.x
[7]  Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315: 531–534. doi: 10.1126/science.1135926
[8]  Liao Y, Tang J, Deng Q, Deng Y, Luo T, et al. (2011) Bilateral fronto-parietal integrity in young chronic cigarette smokers: A diffusion tensor imaging study. PloS one 6: e26460. doi: 10.1371/journal.pone.0026460
[9]  Yu R, Zhao L, Lu L (2011) Regional Grey and White Matter Changes in Heavy Male Smokers. PloS one 6: e27440. doi: 10.1371/journal.pone.0027440
[10]  Ernst M, Matochik JA, Heishman SJ, Van Horn JD, Jons PH, et al. (2001) Effect of nicotine on brain activation during performance of a working memory task. Proceedings of the National Academy of Sciences 98: 4728–4733. doi: 10.1073/pnas.061369098
[11]  Xu J, Mendrek A, Cohen MS, Monterosso J, Rodriguez P, et al. (2005) Brain activity in cigarette smokers performing a working memory task: effect of smoking abstinence. Biological psychiatry 58: 143. doi: 10.1016/j.biopsych.2005.03.028
[12]  Luo S, Ainslie G, Giragosian L, Monterosso JR (2011) Striatal hyposensitivity to delayed rewards among cigarette smokers. Drug and alcohol dependence 116: 18–23. doi: 10.1016/j.drugalcdep.2010.11.012
[13]  Azizian A, Nestor LJ, Payer D, Monterosso JR, Brody AL, et al. (2009) Smoking reduces conflict-related anterior cingulate activity in abstinent cigarette smokers performing a Stroop task. Neuropsychopharmacology 35: 775–782. doi: 10.1038/npp.2009.186
[14]  Gons RA, van Norden AG, de Laat KF, van Oudheusden LJ, van Uden IW, et al. (2011) Cigarette smoking is associated with reduced microstructural integrity of cerebral white matter. Brain 134: 2116–2124. doi: 10.1093/brain/awr145
[15]  Hudkins M, O'Neill J, Tobias MC, Bartzokis G, London ED (2012) Cigarette smoking and white matter microstructure. Psychopharmacology: 1–11.
[16]  Pan P, Shi H, Zhong J, Xiao P, Shen Y, et al.. (2012) Chronic smoking and brain gray matter changes: evidence from meta-analysis of voxel-based morphometry studies. Neurological Sciences: 1–5.
[17]  Stein EA, Pankiewicz J, Harsch HH, Cho J-K, Fuller SA, et al. (1998) Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. American Journal of Psychiatry 155: 1009–1015.
[18]  Lawrence NS, Ross TJ, Stein EA (2002) Cognitive mechanisms of nicotine on visual attention. Neuron 36: 539. doi: 10.1016/s0896-6273(02)01004-8
[19]  Hahn B, Ross TJ, Yang Y, Kim I, Huestis MA, et al. (2007) Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network. The Journal of Neuroscience 27: 3477–3489. doi: 10.1523/jneurosci.5129-06.2007
[20]  Cole DM, Beckmann CF, Long CJ, Matthews PM, Durcan MJ, et al. (2010) Nicotine replacement in abstinent smokers improves cognitive withdrawal symptoms with modulation of resting brain network dynamics. Neuroimage 52: 590–599. doi: 10.1016/j.neuroimage.2010.04.251
[21]  Tanabe J, Nyberg E, Martin LF, Martin J, Cordes D, et al. (2011) Nicotine effects on default mode network during resting state. Psychopharmacology 216: 287–295. doi: 10.1007/s00213-011-2221-8
[22]  Poorthuis RB, Goriounova NA, Couey JJ, Mansvelder HD (2009) Nicotinic actions on neuronal networks for cognition: general principles and long-term consequences. Biochemical pharmacology 78: 668–676. doi: 10.1016/j.bcp.2009.04.031
[23]  Raichle ME, Snyder AZ (2007) A default mode of brain function: a brief history of an evolving idea. Neuroimage 37: 1083–1090. doi: 10.1016/j.neuroimage.2007.02.041
[24]  Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience 8: 700–711. doi: 10.1038/nrn2201
[25]  Yu R, Zhao L, Tian J, Qin W, Wang W, et al. (2011) Regional homogeneity changes in heavy male smokers: a resting-state functional magnetic resonance imaging study. Addiction Biology 18: 729–731. doi: 10.1111/j.1369-1600.2011.00359.x
[26]  West R, Ussher M (2010) Is the ten-item Questionnaire of Smoking Urges (QSU-brief) more sensitive to abstinence than shorter craving measures? Psychopharmacology 208: 427–432. doi: 10.1007/s00213-009-1742-x
[27]  Cox LS, Tiffany ST, Christen AG (2001) Evaluation of the brief questionnaire of smoking urges (QSU-brief) in laboratory and clinical settings. Nicotine & Tobacco Research 3: 7–16. doi: 10.1080/14622200124218
[28]  Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11: 805–821. doi: 10.1006/nimg.2000.0582
[29]  Takeuchi H, Taki Y, Sassa Y, Hashizume H, Sekiguchi A, et al. (2012) Brain structures associated with executive functions during everyday events in a non-clinical sample. Brain Structure and Function 218: 1–16. doi: 10.1007/s00429-012-0444-z
[30]  Takeuchi H, Taki Y, Nouchi R, Sekiguchi A, Kotozaki Y, et al. (2012) Regional gray matter density is associated with achievement motivation: evidence from voxel-based morphometry. Brain Structure and Function 219: 1–13. doi: 10.1007/s00429-012-0485-3
[31]  Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, et al. (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. The Journal of Neuroscience 29: 1860–1873. doi: 10.1523/jneurosci.5062-08.2009
[32]  Tomasi D, Volkow ND (2010) Functional connectivity density mapping. Proceedings of the National Academy of Sciences 107: 9885–9890. doi: 10.1073/pnas.1001414107
[33]  Tomasi D, Volkow ND (2012) Gender differences in brain functional connectivity density. Human brain mapping 33: 849–860. doi: 10.1002/hbm.21252
[34]  Tomasi D, Volkow ND (2011) Association between functional connectivity hubs and brain networks. Cerebral Cortex 21: 2003–2013. doi: 10.1093/cercor/bhq268
[35]  Wood D, Mould M, Ong S, Baker E (2005) “Pack year” smoking histories: what about patients who use loose tobacco? Tobacco control 14: 141–142. doi: 10.1136/tc.2004.009977
[36]  Duan X, He S, Liao W, Liang D, Qiu L, et al. (2012) Reduced caudate volume and enhanced striatal-DMN integration in chess experts. Neuroimage 60: 1280–1286. doi: 10.1016/j.neuroimage.2012.01.047
[37]  Morales AM, Ghahremani D, Kohno M, Hellemann GS, London ED (2014) Cigarette Exposure, Dependence, and Craving Are Related to Insula Thickness in Young Adult Smokers. Neuropsychopharmacology 39: 1816–1822. doi: 10.1038/npp.2014.48
[38]  Durazzo TC, Gazdzinski S, Meyerhoff DJ (2007) The neurobiological and neurocognitive consequences of chronic cigarette smoking in alcohol use disorders. Alcohol and alcoholism 42: 174–185. doi: 10.1093/alcalc/agm020
[39]  Picard F, Sadaghiani S, Leroy C, Courvoisier DS, Maroy R, et al. (2013) High density of nicotinic receptors in the cingulo-insular network. Neuroimage 79: 42–51. doi: 10.1016/j.neuroimage.2013.04.074
[40]  Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends in neurosciences 32: 56–67. doi: 10.1016/j.tins.2008.09.009
[41]  Singer T, Critchley HD, Preuschoff K (2009) A common role of insula in feelings, empathy and uncertainty. Trends in cognitive sciences 13: 334–340. doi: 10.1016/j.tics.2009.05.001
[42]  Rose JE, McClernon FJ, Froeliger B, Behm FM, Preud'homme X, et al. (2011) Repetitive transcranial magnetic stimulation of the superior frontal gyrus modulates craving for cigarettes. Biological psychiatry 70: 794–799. doi: 10.1016/j.biopsych.2011.05.031
[43]  Gong G, He Y, Concha L, Lebel C, Gross DW, et al. (2009) Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex 19: 524–536. doi: 10.1093/cercor/bhn102
[44]  Taylor KS, Seminowicz DA, Davis KD (2009) Two systems of resting state connectivity between the insula and cingulate cortex. Human brain mapping 30: 2731–2745. doi: 10.1002/hbm.20705
[45]  Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, et al. (2002) Brain metabolic changes during cigarette craving. Archives of general psychiatry 59: 1162. doi: 10.1001/archpsyc.59.12.1162
[46]  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. Applied psychophysiology and biofeedback 30: 195–204. doi: 10.1007/s10484-005-6377-z
[47]  Thiel CM, Zilles K, Fink GR (2005) Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology 30: 810–820. doi: 10.1038/sj.npp.1300633
[48]  Thiel C, Fink G (2008) Effects of the cholinergic agonist nicotine on reorienting of visual spatial attention and top-down attentional control. Neuroscience 152: 381–390. doi: 10.1016/j.neuroscience.2007.10.061
[49]  Jasinska AJ, Zorick T, Brody AL, Stein EA (2013) Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans. Neuropharmacology 84: 111–122. doi: 10.1016/j.neuropharm.2013.02.015
[50]  Mckiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR (2003) A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience 15: 394–408. doi: 10.1162/089892903321593117
[51]  Whitfield-Gabrieli S, Ford JM (2012) Default mode network activity and connectivity in psychopathology. Annual Review of Clinical Psychology 8: 49–76. doi: 10.1146/annurev-clinpsy-032511-143049
[52]  Anticevic A, Repovs G, Shulman GL, Barch DM (2010) When less is more: TPJ and default network deactivation during encoding predicts working memory performance. Neuroimage 49: 2638–2648. doi: 10.1016/j.neuroimage.2009.11.008
[53]  Daselaar S, Prince S, Cabeza R (2004) When less means more: deactivations during encoding that predict subsequent memory. Neuroimage 23: 921–927. doi: 10.1016/j.neuroimage.2004.07.031
[54]  Weissman D, Roberts K, Visscher K, Woldorff M (2006) The neural bases of momentary lapses in attention. Nature neuroscience 9: 971–978. doi: 10.1038/nn1727
[55]  Anticevic A, Cole MW, Murray JD, Corlett PR, Wang X-J, et al. (2012) The role of default network deactivation in cognition and disease. Trends in cognitive sciences 16: 584–592. doi: 10.1016/j.tics.2012.10.008
[56]  Fields C (2011) From “Oh, OK” to “Ah, yes” to “Aha!”: Hyper-systemizing and the rewards of insight. Personality and Individual Differences 50: 1159–1167. doi: 10.1016/j.paid.2011.02.010
[57]  Heishman SJ, Kleykamp BA, Singleton EG (2010) Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology 210: 453–469. doi: 10.1007/s00213-010-1848-1
[58]  Kwaasteniet Bd, Ruhe E, Caan M, Rive M, Olabarriaga S, et al. (2013) Relation Between Structural and Functional Connectivity in Major DepressiveDisorder. Biological psychiatry 74: 40–47. doi: 10.1016/j.biopsych.2012.12.024
[59]  Steffens DC, Taylor WD, Denny KL, Bergman SR, Wang L (2011) Structural integrity of the uncinate fasciculus and resting state functional connectivity of the ventral prefrontal cortex in late life depression. PloS one 6: e22697. doi: 10.1371/journal.pone.0022697
[60]  Quigley M, Cordes D, Turski P, Moritz C, Haughton V, et al. (2003) Role of the corpus callosum in functional connectivity. American journal of neuroradiology 24: 208–212.
[61]  Johnston JM, Vaishnavi SN, Smyth MD, Zhang D, He BJ, et al. (2008) Loss of resting interhemispheric functional connectivity after complete section of the corpus callosum. The Journal of Neuroscience 28: 6453–6458. doi: 10.1523/jneurosci.0573-08.2008
[62]  Swan GE, Lessov-Schlaggar CN (2007) The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychology review 17: 259–273. doi: 10.1007/s11065-007-9035-9
[63]  Rose JE, Behm FM, Westman EC, Mathew RJ, London ED, et al. (2003) PET studies of the influences of nicotine on neural systems in cigarette smokers. American Journal of Psychiatry 160: 323–333. doi: 10.1176/appi.ajp.160.2.323
[64]  Xu J, Mendrek A, Cohen MS, Monterosso J, Simon S, et al. (2006) Effect of cigarette smoking on prefrontal cortical function in nondeprived smokers performing the Stroop Task. Neuropsychopharmacology 32: 1421–1428. doi: 10.1038/sj.npp.1301272
[65]  Miller LR, Mukherjee S, Ansah TA, Das SK (2007) Cigarette smoke and dopaminergic system. Journal of biochemical and molecular toxicology 21: 325–335. doi: 10.1002/jbt.20197

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