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Nicotine in action: cigarette smoking modulated homotopic functional connectivity in schizophrenia

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Abstract

Cigarette smoking is intimately associated with both early onset and increased severity of schizophrenia. The self-medication hypothesis suggests that nicotine can relieve or restore neurocognitive deficits and symptoms associated with schizophrenia. Schizophrenia patients and healthy subjects who smoked showed deficits in communication between their hemispheres. These homotopic connectivity mechanisms associated with both schizophrenia and smoking comorbidity were largely unknown until now. A mixed sample including patients with schizophrenia (22 smokers and 27 non-smokers) and healthy controls (22 smokers and 21 non-smokers) based on clinical diagnoses and cigarette dependence were recruited for the current study. All subjects underwent resting-state functional magnetic resonance imaging to determine possible interactions between schizophrenia and smoking, and to determine the main effects of schizophrenia and smoking on homotopic functional connectivity. Decreased homotopic functional connectivity of the subgenual anterior cingulate cortex suggested a main effect of schizophrenia and smoking—an additive effect. Furthermore, we found an antagonistic interaction effect between schizophrenia and smoking located in the ventrolateral prefrontal cortex (VLPFC). In addition, the connectivity strength of the bilateral VLPFC was negatively correlated with the Positive and Negative Syndrome Scale Negative scores and positively correlated with lifetime smoking. These results suggest that smoking has multiple effects on the modulation of interhemispheric connectivity in schizophrenia. Our findings provide valuable information underlying the pathophysiological mechanisms of schizophrenia and offer a potential target for future clinical treatment of schizophrenia and smoking comorbidity.

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References

  • Addicott, M. A., Sweitzer, M. M., Froeliger, B., Rose, J. E., & McClernon, F. J. (2015). Increased functional connectivity in an insula-based network is associated with improved smoking cessation outcomes. Neuropsychopharmacology, 40(11), 2648–2656. https://doi.org/10.1038/npp.2015.114.

    Article  PubMed  PubMed Central  Google Scholar 

  • Adler, L. E., Olincy, A., Waldo, M., Harris, J. G., Griffith, J., Stevens, K., Flach, K., Nagamoto, H., Bickford, P., Leonard, S., & Freedman, R. (1998). Schizophrenia, sensory gating, and nicotinic receptors. Schizophrenia Bulletin, 24(2), 189–202.

    Article  CAS  PubMed  Google Scholar 

  • Andreasen, N. C., Pressler, M., Nopoulos, P., Miller, D., & Ho, B. C. (2010). Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biological Psychiatry, 67(3), 255–262. https://doi.org/10.1016/j.biopsych.2009.08.040.

    Article  CAS  PubMed  Google Scholar 

  • Badre, D., & Wagner, A. D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45(13), 2883–2901.

    Article  PubMed  Google Scholar 

  • Baker, J. T., Holmes, A. J., Masters, G. A., Yeo, B. T., Krienen, F., Buckner, R. L., et al. (2014). Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. JAMA Psychiatry, 71(2), 109–118. https://doi.org/10.1001/jamapsychiatry.2013.3469.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bersani, G., Quartini, A., Iannitelli, A., Paolemili, M., Ratti, F., Di Biasi, C., et al. (2010). Corpus callosum abnormalities and potential age effect in men with schizophrenia: an MRI comparative study. Psychiatry Research, 183(2), 119–125. https://doi.org/10.1016/j.pscychresns.2010.04.011.

    Article  PubMed  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews. Neuroscience, 10(3), 186–198. https://doi.org/10.1038/nrn2575.

    Article  CAS  PubMed  Google Scholar 

  • Camchong, J., MacDonald III, A. W., Bell, C., Mueller, B. A., & Lim, K. O. (2009). Altered functional and anatomical connectivity in schizophrenia. Schizophrenia Bulletin, 37(3), 640–650.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang, X., Xi, Y. B., Cui, L. B., Wang, H. N., Sun, J. B., Zhu, Y. Q., et al. (2015). Distinct inter-hemispheric dysconnectivity in schizophrenia patients with and without auditory verbal hallucinations. Scientific Reports, 5, 11218.

  • Chen, X., Lu, B., & Yan, C. G. (2017). Reproducibility of R-fMRI metrics on the impact of different strategies for multiple comparison correction and sample sizes. Human Brain Mapping, 39, 300–318. https://doi.org/10.1002/hbm.23843.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Leon, J., & Diaz, F. J. (2005). A meta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors. Schizophrenia Research, 76(2–3), 135–157. https://doi.org/10.1016/j.schres.2005.02.010.

    Article  PubMed  Google Scholar 

  • de Ruiter, M. B., Veltman, D. J., Goudriaan, A. E., Oosterlaan, J., Sjoerds, Z., & van den Brink, W. (2009). Response perseveration and ventral prefrontal sensitivity to reward and punishment in male problem gamblers and smokers. Neuropsychopharmacology, 34(4), 1027–1038. https://doi.org/10.1038/npp.2008.175.

    Article  PubMed  Google Scholar 

  • DeMyer, M. K., Gilmor, R. L., Hendrie, H. C., DeMyer, W. E., Augustyn, G. T., & Jackson, R. K. (1988). Magnetic resonance brain images in schizophrenic and normal subjects: influence of diagnosis and education. Schizophrenia Bulletin, 14(1), 21–37.

    Article  CAS  PubMed  Google Scholar 

  • Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America, 113(28), 7900–7905. https://doi.org/10.1073/pnas.1602413113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox, M. D., Buckner, R. L., Liu, H., Chakravarty, M. M., Lozano, A. M., & Pascual-Leone, A. (2014). Resting-state networks link invasive and noninvasive brain stimulation across diverse psychiatric and neurological diseases. Proceedings of the National Academy of Sciences of the United States of America, 111(41), E4367–E4375. https://doi.org/10.1073/pnas.1405003111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346–355.

    Article  CAS  PubMed  Google Scholar 

  • Galvan, A., Poldrack, R. A., Baker, C. M., McGlennen, K. M., & London, E. D. (2011). Neural correlates of response inhibition and cigarette smoking in late adolescence. Neuropsychopharmacology, 36(5), 970–978. https://doi.org/10.1038/npp.2010.235.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein, R. Z., & Volkow, N. D. (2011). Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nature Reviews. Neuroscience, 12(11), 652–669. https://doi.org/10.1038/nrn3119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, W., Xiao, C., Liu, G., Wooderson, S. C., Zhang, Z., Zhang, J., Yu, L., & Liu, J. (2014). Decreased resting-state interhemispheric coordination in first-episode, drug-naive paranoid schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 48, 14–19.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Hoptman, M. J., Zuo, X. N., D'Angelo, D., Mauro, C. J., Butler, P. D., Milham, M. P., & Javitt, D. C. (2012). Decreased interhemispheric coordination in schizophrenia: a resting state fMRI study. Schizophrenia Research, 141(1), 1–7.

    Article  PubMed  Google Scholar 

  • Horn, N. R., Dolan, M., Elliott, R., Deakin, J. F., & Woodruff, P. W. (2003). Response inhibition and impulsivity: an fMRI study. Neuropsychologia, 41(14), 1959–1966.

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen, L. K., D'Souza, D. C., Mencl, W. E., Pugh, K. R., Skudlarski, P., & Krystal, J. H. (2004). Nicotine effects on brain function and functional connectivity in schizophrenia. Biological Psychiatry, 55(8), 850–858. https://doi.org/10.1016/j.biopsych.2003.12.023.

    Article  CAS  PubMed  Google Scholar 

  • Jalili, M., Meuli, R., Do, K. Q., Hasler, M., Crow, T. J., & Knyazeva, M. G. (2010). Attenuated asymmetry of functional connectivity in schizophrenia: a high-resolution EEG study. Psychophysiology, 47(4), 706–716. https://doi.org/10.1111/j.1469-8986.2009.00971.x.

    Article  PubMed  Google Scholar 

  • Ji, G. J., Zhang, Z., Xu, Q., Zang, Y. F., Liao, W., & Lu, G. (2014). Generalized tonic-clonic seizures: aberrant interhemispheric functional and anatomical connectivity. Radiology, 271(3), 839–847. https://doi.org/10.1148/radiol.13131638.

    Article  PubMed  Google Scholar 

  • Ji, G. J., Zhang, Z., Xu, Q., Wang, Z., Wang, J., Jiao, Q., Yang, F., Tan, Q., Chen, G., Zang, Y. F., Liao, W., & Lu, G. (2015). Identifying Corticothalamic network epicenters in patients with idiopathic generalized epilepsy. AJNR. American Journal of Neuroradiology, 36(8), 1494–1500. https://doi.org/10.3174/ajnr.A4308.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261–276.

    Article  CAS  PubMed  Google Scholar 

  • Kelly, C., Zuo, X. N., Gotimer, K., Cox, C. L., Lynch, L., Brock, D., Imperati, D., Garavan, H., Rotrosen, J., Castellanos, F. X., & Milham, M. P. (2011). Reduced interhemispheric resting state functional connectivity in cocaine addiction. Biological Psychiatry, 69(7), 684–692. https://doi.org/10.1016/j.biopsych.2010.11.022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan, M. S., Boileau, I., Kolla, N., & Mizrahi, R. (2018). A systematic review of the role of the nociceptin receptor system in stress, cognition, and reward: relevance to schizophrenia. Translational Psychiatry, 8(1), 38. https://doi.org/10.1038/s41398-017-0080-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koukouli, F., Rooy, M., Tziotis, D., Sailor, K. A., O'Neill, H. C., Levenga, J., Witte, M., Nilges, M., Changeux, J. P., Hoeffer, C. A., Stitzel, J. A., Gutkin, B. S., DiGregorio, D. A., & Maskos, U. (2017). Nicotine reverses hypofrontality in animal models of addiction and schizophrenia. Nature Medicine, 23(3), 347–354. https://doi.org/10.1038/nm.4274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krystal, J. H., D'Souza, D. C., Gallinat, J., Driesen, N., Abi-Dargham, A., Petrakis, I., et al. (2006). The vulnerability to alcohol and substance abuse in individuals diagnosed with schizophrenia. Neurotoxicity Research, 10(3–4), 235–252.

    Article  CAS  PubMed  Google Scholar 

  • Leonard, S., Mexal, S., & Freedman, R. (2007). Smoking, genetics and schizophrenia: evidence for self medication. Journal of Dual Diagnosis, 3(3–4), 43–59.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, H. J., Xu, Y., Zhang, K. R., Hoptman, M. J., & Zuo, X. N. (2015). Homotopic connectivity in drug-naive, first-episode, early-onset schizophrenia. Journal of Child Psychology and Psychiatry, 56(4), 432–443.

    Article  PubMed  Google Scholar 

  • Liao, W., Yu, Y., Miao, H. H., Feng, Y. X., Ji, G. J., & Feng, J. H. (2017). Inter-hemispheric intrinsic connectivity as a Neuromarker for the diagnosis of boys with Tourette syndrome. Molecular Neurobiology, 54(4), 2781–2789. https://doi.org/10.1007/s12035-016-9863-9.

    Article  CAS  PubMed  Google Scholar 

  • Lin, F., Wu, G., Zhu, L., & Lei, H. (2013). Heavy smokers show abnormal microstructural integrity in the anterior corpus callosum: a diffusion tensor imaging study with tract-based spatial statistics. Drug and Alcohol Dependence, 129(1), 82–87.

    Article  CAS  PubMed  Google Scholar 

  • Moran, L. V., Sampath, H., Stein, E. A., & Hong, L. E. (2012). Insular and anterior cingulate circuits in smokers with schizophrenia. Schizophrenia Research, 142(1), 223–229.

    Article  PubMed  Google Scholar 

  • Moran, L. V., Sampath, H., Kochunov, P., & Hong, L. E. (2013). Brain circuits that link schizophrenia to high risk of cigarette smoking. Schizophrenia Bulletin, 39(6), 1373–1381. https://doi.org/10.1093/schbul/sbs149.

    Article  PubMed  Google Scholar 

  • Moran, L. V., Betts, J. M., Ongur, D., & Janes, A. C. (2017). Neural responses to smoking cues in schizophrenia. Schizophrenia Bulletin. https://doi.org/10.1093/schbul/sbx1085.

  • Patkar, A. A., Gopalakrishnan, R., Lundy, A., Leone, F. T., Certa, K. M., & Weinstein, S. P. (2002). Relationship between tobacco smoking and positive and negative symptoms in schizophrenia. The Journal of Nervous and Mental Disease, 190(9), 604–610. https://doi.org/10.1097/01.NMD.0000030525.40247.B9.

    Article  PubMed  Google Scholar 

  • Potvin, S., Lungu, O., Lipp, O., Lalonde, P., Zaharieva, V., Stip, E., Melun, J. P., & Mendrek, A. (2016). Increased ventro-medial prefrontal activations in schizophrenia smokers during cigarette cravings. Schizophrenia Research, 173(1–2), 30–36. https://doi.org/10.1016/j.schres.2016.03.011.

    Article  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. https://doi.org/10.1016/j.neuroimage.2011.10.018.

    Article  PubMed  Google Scholar 

  • Resnick, S. M. (1992). Matching for education in studies of schizophrenia. Archives of General Psychiatry, 49(3), 246.

    Article  CAS  PubMed  Google Scholar 

  • Ribolsi, M., Koch, G., Magni, V., Di Lorenzo, G., Rubino, I. A., Siracusano, A., et al. (2009). Abnormal brain lateralization and connectivity in schizophrenia. Reviews in the Neurosciences, 20(1), 61–70.

    Article  PubMed  Google Scholar 

  • Roland, J. L., Snyder, A. Z., Hacker, C. D., Mitra, A., Shimony, J. S., Limbrick, D. D., Raichle, M. E., Smyth, M. D., & Leuthardt, E. C. (2017). On the role of the corpus callosum in interhemispheric functional connectivity in humans. Proceedings of the National Academy of Sciences of the United States of America, 114, 13278–13283. https://doi.org/10.1073/pnas.1707050114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossi, A., Stratta, P., di Michele, V., de Cataldo, S., & Cassacchia, M. (1991). Lateral ventricular size, educational level and patient subtypes in schizophrenia. The British Journal of Psychiatry, 159, 443–444.

    Article  CAS  PubMed  Google Scholar 

  • Saliba, M., Assaad, S., Haddad, C., Hallit, S., Hachem, D., & Haddad, G. (2017). Schizophrenia and smoking: impact on negative symptoms. Revista inteRnacional de investigación en adicciones, 1, 28–35.

    Article  Google Scholar 

  • Savjani, R. R., Velasquez, K. M., Thompson-Lake, D. G. Y., Baldwin, P. R., Eagleman, D. M., De La Garza II, R., et al. (2014). Characterizing white matter changes in cigarette smokers via diffusion tensor imaging. Drug and Alcohol Dependence, 145, 134–142.

    Article  PubMed  Google Scholar 

  • Schuepbach, D., Keshavan, M. S., Kmiec, J. A., & Sweeney, J. A. (2002). Negative symptom resolution and improvements in specific cognitive deficits after acute treatment in first-episode schizophrenia. Schizophrenia Research, 53(3), 249–261.

    Article  PubMed  Google Scholar 

  • Schwartz, R. C. (2007). Concurrent validity of the global assessment of functioning scale for clients with schizophrenia. Psychological Reports, 100(2), 571–574. https://doi.org/10.2466/pr0.100.2.571-574.

    Article  PubMed  Google Scholar 

  • Schwarzkopf, D. S., De Haas, B., & Rees, G. (2012). Better ways to improve standards in brain-behavior correlation analysis. Frontiers in Human Neuroscience, 6, 200. https://doi.org/10.3389/fnhum.2012.00200.

    Article  PubMed  PubMed Central  Google Scholar 

  • Smucny, J., Olincy, A., & Tregellas, J. R. (2016). Nicotine restores functional connectivity of the ventral attention network in schizophrenia. Neuropharmacology, 108, 144–151. https://doi.org/10.1016/j.neuropharm.2016.04.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturmer, T., Glynn, R. J., Lee, I. M., Christen, W. G., & Hennekens, C. H. (2000). Lifetime cigarette smoking and colorectal cancer incidence in the Physicians' health study I. Journal of the National Cancer Institute, 92(14), 1178–1181.

    Article  CAS  PubMed  Google Scholar 

  • Viswanath, H., Velasquez, K. M., Thompson-Lake, D. G., Savjani, R., Carter, A. Q., Eagleman, D., et al. (2015). Alterations in interhemispheric functional and anatomical connectivity are associated with tobacco smoking in humans. Front Hum Neurosci, 9, https://doi.org/10.3389/fnhum.2015.00116.

  • Walterfang, M., Wood, A. G., Reutens, D. C., Wood, S. J., Chen, J., Velakoulis, D., McGorry, P. D., & Pantelis, C. (2008). Morphology of the corpus callosum at different stages of schizophrenia: cross-sectional study in first-episode and chronic illness. The British Journal of Psychiatry, 192(6), 429–434. https://doi.org/10.1192/bjp.bp.107.041251.

    Article  PubMed  Google Scholar 

  • Walterfang, M., Wood, A. G., Reutens, D. C., Wood, S. J., Chen, J., Velakoulis, D., McGorry, P. D., & Pantelis, C. (2009). Corpus callosum size and shape in first-episode affective and schizophrenia-spectrum psychosis. Psychiatry Research, 173(1), 77–82. https://doi.org/10.1016/j.pscychresns.2008.09.007.

    Article  PubMed  Google Scholar 

  • Winterer, G. (2010). Why do patients with schizophrenia smoke? Current Opinion in Psychiatry, 23(2), 112–119. https://doi.org/10.1097/YCO.0b013e3283366643.

    Article  PubMed  Google Scholar 

  • Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: Data Processing & Analysis for (resting-state) brain imaging. Neuroinformatics, 14(3), 339–351. https://doi.org/10.1007/s12021-016-9299-4.

    Article  PubMed  Google Scholar 

  • Yang, G. J., Murray, J. D., Repovs, G., Cole, M. W., Savic, A., Glasser, M. F., Pittenger, C., Krystal, J. H., Wang, X. J., Pearlson, G. D., Glahn, D. C., & Anticevic, A. (2014). Altered global brain signal in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 111(20), 7438–7443. https://doi.org/10.1073/pnas.1405289111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, G. J., Murray, J. D., Glasser, M., Pearlson, G. D., Krystal, J. H., Schleifer, C., Repovs, G., & Anticevic, A. (2017). Altered global signal topography in schizophrenia. Cerebral Cortex, 27(11), 5156–5169. https://doi.org/10.1093/cercor/bhw297.

    Article  PubMed  Google Scholar 

  • Yokoyama, N., Sasaki, H., Mori, Y., Ono, M., Tsurumi, K., Kawada, R., Matsumoto, Y., Yoshihara, Y., Sugihara, G., Miyata, J., Murai, T., & Takahashi, H. (2017). Additive effect of cigarette smoking on gray matter abnormalities in schizophrenia. Schizophrenia Bulletin. https://doi.org/10.1093/schbul/sbx1092.

  • Yu, D., Yuan, K., Bi, Y., Luo, L., Zhai, J., Liu, B., et al. (2017). Altered interhemispheric resting-state functional connectivity in young male smokers. Addiction Biology, 23(2), 772–780.

    Article  PubMed  Google Scholar 

  • Zhang, X., Stein, E. A., & Hong, L. E. (2010). Smoking and schizophrenia independently and additively reduce white matter integrity between striatum and frontal cortex. Biological Psychiatry, 68(7), 674–677. https://doi.org/10.1016/j.biopsych.2010.06.018.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, R., Wei, Q., Kang, Z., Zalesky, A., Li, M., Xu, Y., Li, L., Wang, J., Zheng, L., Wang, B., Zhao, J., Zhang, J., & Huang, R. (2015). Disrupted brain anatomical connectivity in medication-naive patients with first-episode schizophrenia. Brain Structure & Function, 220(2), 1145–1159. https://doi.org/10.1007/s00429-014-0706-z.

    Article  CAS  Google Scholar 

  • Zuo, X. N., Kelly, C., Di Martino, A., Mennes, M., Margulies, D. S., Bangaru, S., et al. (2010). Growing together and growing apart: Regional and sex differences in the lifespan developmental trajectories of functional homotopy. The Journal of Neuroscience, 30(45), 15034–15043. https://doi.org/10.1523/JNEUROSCI.2612-10.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (61533006, 81471653, 81771919 and 61673089), China Postdoctoral Science Foundation (2013 M532229), Sichuan Science and Technology Program (2018TJPT0016), and the “111” project (B12027).

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Liao, W., Yang, S., Li, J. et al. Nicotine in action: cigarette smoking modulated homotopic functional connectivity in schizophrenia. Brain Imaging and Behavior 13, 1612–1623 (2019). https://doi.org/10.1007/s11682-018-0001-3

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