Nicotine replacement in abstinent smokers improves cognitive withdrawal symptoms with modulation of resting brain network dynamics

NeuroImage

Volumn 52, Issue 2, 2010, Pages 590-599

  Cole, David M ^a,b   Beckmann, Christian F ^a,c   Long, Christopher J ^a,b   Matthews, Paul M ^a,b   Durcan, Michael J ^d   Beaver, John D ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Cognition; Default mode; Executive control; FMRI; Functional connectivity; Independent component analysis; Networks; Nicotine; Resting state; Withdrawal

Indexed keywords

NICOTINE; PLACEBO; NICOTINIC AGENT;

ADULT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; CLINICAL TRIAL; COGNITION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NEUROMODULATION; NICOTINE REPLACEMENT THERAPY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REWARD; SMOKING CESSATION; TOBACCO DEPENDENCE; WITHDRAWAL SYNDROME; BRAIN; BRAIN MAPPING; COGNITION DISORDERS; COMPLICATION; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; EXECUTIVE FUNCTION; MIDDLE AGED; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOKING; SUBSTANCE WITHDRAWAL SYNDROME; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; COGNITION DISORDERS; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; EXECUTIVE FUNCTION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; NICOTINE; NICOTINIC AGONISTS; SMOKING; SUBSTANCE WITHDRAWAL SYNDROME; YOUNG ADULT;

EID: 77953725584     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.04.251     Document Type: Article

References (65)

1. Albert N.B., Robertson E.M., Miall R.C. The resting human brain and motor learning. Curr. Biol. 2009, 19:1023-1027.
2. Anand A., Li Y., Wang Y., Wu J., Gao S., Bukhari L., Mathews V.P., Kalnin A., Lowe M.J. Antidepressant effect on connectivity of the mood-regulating circuit: an fMRI study. Neuropsychopharmacology 2005, 30:1334-1344.
3. Andersson J., Smith S., Jenkinson M. FNIRT-FMRIB's non-linear image registration tool. 14th Annual Meeting of the Organization for Human Brain Mapping 2008, poster 496 [abstr].
4. Atzori G., Lemmonds C.A., Kotler M.L., Durcan M.J., Boyle J. Efficacy of a nicotine (4mg)-containing lozenge on the cognitive impairment of nicotine withdrawal. J. Clin. Psychopharmacol. 2008, 28:667-674.
5. Baliki M.N., Geha P.Y., Apkarian A.V., Chialvo D.R. Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. J. Neurosci. 2008, 28:1398-1403.
6. Beckmann C.F., Smith S.M. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 2004, 23:137-152.
7. Beckmann C.F., Smith S.M. Tensorial extension of independent component analysis for multisubject fMRI analysis. NeuroImage 2005, 25:294-311.
8. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:1001-1013.
9. Beckmann C.F., Mackay C.E., Filippini N., Smith S.M. Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. 15th Annual Meeting of the Organization for Human Brain Mapping 2009, poster 441 SU-AM [abstr].
10. Bell S.L., Taylor R.C., Singleton E.G., Henningfield J.E., Heishman S.J. Smoking after nicotine deprivation enhances cognitive performance and decreases tobacco craving in drug abusers. Nicotine Tob. Res. 1999, 1:45-52.
11. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
12. Castellanos F.X., Margulies D.S., Kelly C., Uddin L.Q., Ghaffari M., Kirsch A., Shaw D., Shehzad Z., Di Martino A., Biswal B., Sonuga-Barke E.J., Rotrosen J., Adler L.A., Milham M.P. Cingulate-precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry 2008, 63:332-337.
13. Chang C., Glover G.H. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. NeuroImage 2009, Electronic publication ahead of print. 10.1016/j.neuroimage.2009.12.011.
14. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
15. Damoiseaux J.S., Beckmann C.F., Arigita E.J., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Rombouts S.A. Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18:1856-1864.
16. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E., Schlaggar B.L., Petersen S.E. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11073-11078.
17. Filippini N., Macintosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of activation in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7209-7214.
18. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
19. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organised into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
20. Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007, 56:171-184.
21. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 2009, 101:3270-3283.
22. Frodl T., Bokde A.L., Scheuerecker J., Lisiecka D., Schoepf V., Hampel H., Moller H.J., Bruckmann H., Wiesmann M., Meisenzahl E. Functional connectivity bias of the orbitofrontal cortex in drug-free patients with major depression. Biol. Psychiatry 2010, 67:161-167.
23. Froeliger B., Gilbert D.G., McClernon F.J. Effects of nicotine on novelty detection and memory recognition performance: double-blind, placebo-controlled studies of smokers and nonsmokers. Psychopharmacology (Berl.) 2009, 205:625-633.
24. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:253-258.
25. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4637-4642.
26. Gusnard D.A., Raichle M.E. Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2001, 2:685-694.
27. Gusnard D.A., Akbudak E., Shulman G.L., Raichle M.E. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4259-4264.
28. Hahn B., Ross T.J., Yang Y., Kim I., Huestis M.A., Stein E.A. Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network. J. Neurosci. 2007, 27:3477-3489.
29. Hahn B., Ross T.J., Wolkenberg F.A., Shakleya D.M., Huestis M.A., Stein E.A. Performance effects of nicotine during selective attention, divided attention, and simple stimulus detection: an fMRI study. Cereb. Cortex 2009, 19:1990-2000.
30. Heatherton T.F., Kozlowski L.T., Frecker R.C., Fagerström K.O. The Fagerström test for nicotine dependence: a revision of the Fagerström tolerance questionnaire. Br. J. Addict. 1991, 86:1119-1127.
31. Heishman S.J., Taylor R.C., Henningfield J.E. Nicotine and smoking: a review of effects on human performance. Exp. Clin. Psychopharmacol. 1994, 2:345-395.
32. Hong L.E., Gu H., Yang Y., Ross T.J., Salmeron B.J., Buchholz B., Thaker G.K., Stein E.A. Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. Arch. Gen. Psychiatry 2009, 66:431-441.
33. Hughes J.R. Tobacco withdrawal in self-quitters. J. Consult. Clin. Psychol. 1992, 60:689-697.
34. Hughes J.R., Hatsukami D. Signs and symptoms of tobacco withdrawal. Arch. Gen. Psychiatry 1986, 43:289-294.
35. Hughes J.R., Higgins S.T., Bickel W.K. Nicotine withdrawal versus other drug withdrawal syndromes: similarities and dissimilarities. Addiction 1994, 89:1461-1470.
36. Hyland A., Rezaishiraz H., Giovino G., Bauer J.E., Cummings K.M. Over-the-counter availability of nicotine replacement therapy and smoking cessation. Nicotine Tob. Res. 2005, 7:547-555.
37. Jenkinson M., Bannister P.R., Brady J.M., Smith S.M. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002, 17:825-841.
38. Kelly A.M.C., Uddin L.Q., Biswal B.B., Castellanos F.X., Milham M.P. Competition between functional brain networks mediates behavioural variability. NeuroImage 2008, 39:527-537.
39. Kenney J.W., Gould T.J. Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol. Neurobiol. 2008, 38:101-121.
40. Kiviniemi V., Starck T., Remes J., Long X., Nikkinen J., Haapea M., Veijola J., Moilanen I., Isohanni M., Zang Y.F., Tervonen O. Functional segmentation of the brain cortex using high model order group PICA. Hum. Brain Mapp. 2009, 30:3865-3886.
41. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35:217-238.
42. Kringelbach M.L., Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 2004, 72:341-372.
43. Lawrence N.S., Ross T.J., Stein E.A. Cognitive mechanisms of nicotine on visual attention. Neuron 2002, 36:539-548.
44. Lawrence N.S., Ross T.J., Hoffman R., Garavan H., Stein E.A. Multiple neuronal networks mediate sustained attention. J. Cogn. Neurosci. 2003, 15:1028-1038.
45. Mansvelder H.D., van Aerde K.I., Couey J.J., Brussaard A.B. Nicotinic modulation of neuronal networks: from receptors to cognition. Psychopharmacology (Berl.) 2006, 184:292-305.
46. Mantini D., Perrucci M.G., Del Gratta C., Romani G.L., Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13170-13175.
47. Mathew R.J., Wilson W.H. Substance abuse and cerebral blood flow. Am. J. Psychiatry 1991, 148:292-305.
48. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. NeuroImage 2009, 44:893-905.
49. Naqvi N.H., Rudrauf D., Damasio H., Bechara A. Damage to the insula disrupts cigarette smoking. Science 2007, 315:531-534.
50. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
51. O'Doherty J.P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 2004, 14:769-776.
52. Parrott A.C., Roberts G. Smoking deprivation and cigarette reinstatement: effects upon visual attention. J. Psychopharmacol. 1991, 5:404-409.
53. Parrott A.C., Garnham N.J., Wesnes K., Pincock C. Cigarette smoking and abstinence: comparative effects upon cognitive task performance and mood state over 24hours. Hum. Psychopharmacol. 1996, 11:391-400.
54. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
55. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., Greicius M.D. Neurodegenerative diseases target large-scale functional brain networks. Neuron 2009, 62:42-52.
56. Shulman G.L., Fiez J.A., Corbetta M., Buckner R.L., Miezin F.M., Raichle M.E., Petersen S.E. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 1997, 9:648-663.
57. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
58. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
59. Sridharan D., Levitin D.J., Menon V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12569-12574.
60. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 2006, 96:3517-3531.
61. Wang K., Liang M., Wang L., Tian L., Zhang X., Li K., Jiang T. Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum. Brain Mapp. 2007, 28:967-978.
62. Wang Z., Faith M., Patterson F., Tang K., Kerrin K., Wileyto E.P., Detre J.A., Lerman C. Neural substrates of abstinence-induced cigarette cravings in chronic smokers. J. Neurosci. 2007, 27:14035-14040.
63. Xu J., Mendrek A., Cohen M.S., Monterosso J., Rodriguez P., Simon S.L., Brody A., Jarvik M., Domier C.P., Olmstead R., Ernst M., London E.D. Brain activity in cigarette smokers performing a working memory task: effect of smoking abstinence. Biol. Psychiatry 2005, 58:143-150.
64. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.
65. Zuo X.N., Kelly C., Adelstein J.S., Klein D.F., Castellanos F.X., Milham M.P. Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. NeuroImage 2010, 49:2163-2177.