Effects of acute nicotine on brain function in healthy smokers and non-smokers: Estimation of inter-individual response heterogeneity

NeuroImage

Volumn 45, Issue 2, 2009, Pages 549-561

  Ettinger, Ulrich ^a   Williams, Steven C R ^a   Patel, Dhanesh ^a   Michel, Tanja M ^b   Nwaigwe, Agwawumma ^a   Caceres, Alejandro ^a   Mehta, Mitul A ^a   Anilkumar, Anantha P ^a,c   Kumari, Veena ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Acetylcholine; Drug response; fMRI; Heterogeneity; Nicotine; Oculomotor control; Reliability

Indexed keywords

NICOTINE;

ADULT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; EYE MOVEMENT CONTROL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; NORMAL HUMAN; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SMOKING; TASK PERFORMANCE;

ADULT; BRAIN; EVOKED POTENTIALS; EYE MOVEMENTS; FEMALE; HUMANS; INJECTIONS, SUBCUTANEOUS; MALE; NICOTINE; REFLEX; SMOKING;

EID: 60149090888     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.12.029     Document Type: Article

References (66)

1. Amiez C., Kostopoulos P., Champod A.S., and Petrides M. Local morphology predicts functional organization of the dorsal premotor region in the human brain. J. Neurosci. 26 (2006) 2724-2731
2. Berrettini W.H., and Lerman C.E. Pharmacotherapy and pharmacogenetics of nicotine dependence. Am. J. Psychiatry 162 (2005) 1441-1451
3. Borsook D., Bleakman D., Hargreaves R., Upadhyay J., Schmidt K.F., and Becerra L. A 'BOLD' experiment in defining the utility of fMRI in drug development. Neuroimage 42 (2008) 461-466
4. Brett, M., Anton, J.L., Valabregue, R., Poline, J.B., 2002a. Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2-6, 2002, Sendai, Japan. Neuroimage 15.
5. Brett M., Johnsrude I.S., and Owen A.M. The problem of functional localization in the human brain. Nat. Rev. Neurosci. 3 (2002) 243-249
6. Calkins M.E., Iacono W.G., and Curtis C.E. Smooth pursuit and antisaccade performance evidence trait stability in schizophrenia patients and their relatives. Int. J. Psychophysiol. 49 (2003) 139-146
7. Callicott J.H., Mattay V.S., Verchinski B.A., Marenco S., Egan M.F., and Weinberger D.R. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am. J Psychiatry 160 (2003) 2209-2215
8. de Jongh R., Bolt I., Schermer M., and Olivier B. Botox for the brain: enhancement of cognition, mood and pro-social behavior and blunting of unwanted memories. Neurosci. Biobehav. Rev. 32 (2008) 760-776
9. Dépatie L., O'Driscoll G.A., Holahan A.L., Atkinson V., Thavundayil J.X., Kin N.N., and Lal S. Nicotine and behavioral markers of risk for schizophrenia: a double-blind, placebo-controlled, cross-over study. Neuropsychopharmacology 27 (2002) 1056-1070
10. Ettinger U., and Kumari V. Pharmacological studies of smooth pursuit and antisaccade eye movements in schizophrenia: current status and directions for future research. Curr. Neuropharmacology 1 (2003) 285-300
11. Ettinger U., Kumari V., Crawford T.J., Davis R.E., Sharma T., and Corr P.J. Reliability of smooth pursuit, fixation, and saccadic eye movements. Psychophysiology 40 (2003) 620-628
12. Ettinger U., Picchioni M., Hall M.H., Schulze K., Toulopoulou T., Landau S., Crawford T.J., and Murray R.M. Antisaccade performance in monozygotic twins discordant for schizophrenia: the Maudsley twin study. Am. J. Psychiatry 163 (2006) 543-545
13. Feyerabend C., and Russell M.A. A rapid gas-liquid chromatographic method for the determination of cotinine and nicotine in biological fluids. J. Pharm. Pharmacol. 42 (1990) 450-452
14. Friston K., Holmes A., Poline J.B., Price C.J., and Frith C.D. Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4 (1996) 223-235
15. Garavan H., Kelley D., Rosen A., Rao S.M., and Stein E.A. Practice-related functional activation changes in a working memory task. Microsc. Res. Tech. 51 (2000) 54-63
16. Giessing C., Fink G.R., Rosler F., and Thiel C.M. fMRI data predict individual differences of behavioral effects of nicotine: a partial least square analysis. J. Cogn. Neurosci. 19 (2007) 658-670
17. Gilbert S.J., Dumontheil I., Simons J.S., Frith C.D., and Burgess P.W. Comment on "Wandering minds: the default network and stimulus-independent thought". Science 317 (2007) 43
18. Green J.F., King D.J., and Trimble K.M. Antisaccade and smooth pursuit eye movements in healthy subjects receiving sertraline and lorazepam. J. Psychopharmacol. 14 (2000) 30-36
19. Greenwood T.A., Braff D.L., Light G.A., Cadenhead K.S., Calkins M.E., Dobie D.J., Freedman R., Green M.F., Gur R.E., Gur R.C., Mintz J., Nuechterlein K.H., Olincy A., Radant A.D., Seidman L.J., Siever L.J., Silverman J.M., Stone W.S., Swerdlow N.R., Tsuang D.W., Tsuang M.T., Turetsky B.I., and Schork N.J. Initial heritability analyses of endophenotypic measures for schizophrenia: the consortium on the genetics of schizophrenia. Arch. Gen. Psychiatry 64 (2007) 1242-1250
20. Grosbras M.H., Laird A.R., and Paus T. Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum. Brain Mapp. 25 (2005) 140-154
21. Hahn B., Ross T.J., Yang Y., Kim I., Huestis M.A., and Stein E.A. Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network. J. Neurosci. 27 (2007) 3477-3489
22. Hallett P.E. Primary and secondary saccades to goals defined by instructions. Vision Res. 18 (1978) 1279-1296
23. Hanna S.T. Nicotine effect on cardiovascular system and ion channels. J. Cardiovasc. Pharmacol. 47 (2006) 348-358
24. Heatherton T.F., Kozlowski L.T., Frecker R.C., and Fagerstrom K.O. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br. J. Addict. 86 (1991) 1119-1127
25. Heishman S.J. What aspects of human performance are truly enhanced by nicotine?. Addiction 93 (1998) 317-320
26. Hutton S.B., and Ettinger U. The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43 (2006) 302-313
27. Jacobsen L.K., Gore J.C., Skudlarski P., Lacadie C.M., Jatlow P., and Krystal J.H. Impact of intravenous nicotine on BOLD signal response to photic stimulation. Magn. Reson. Imaging 20 (2002) 141-145
28. Jacobsen L.K., D'Souza D.C., Mencl W.E., Pugh K.R., Skudlarski P., and Krystal J.H. Nicotine effects on brain function and functional connectivity in schizophrenia. Biol. Psychiatry 55 (2004) 850-858
29. Kumari V., and Postma P. Nicotine use in schizophrenia: the self medication hypotheses. Neurosci. Biobehav. Rev. 29 (2005) 1021-1034
30. Kumari V., Gray J.A., ffytche D.H., Mitterschiffthaler M.T., Das M., Zachariah E., Vythelingum G.N., Williams S.C., Simmons A., and Sharma T. Cognitive effects of nicotine in humans: an fMRI study. Neuroimage 19 (2003) 1002-1013
31. Lakier J.B. Smoking and cardiovascular disease. Am. J. Med. 93 (1992) 8S-12S
32. Larrison A.L., Briand K.A., and Sereno A.B. Nicotine improves antisaccade task performance without affecting prosaccades. Hum. Psychopharmacol. 19 (2004) 409-419
33. Larrison-Faucher A.L., Matorin A.A., and Sereno A.B. Nicotine reduces antisaccade errors in task impaired schizophrenic subjects. Prog. Neuropsychopharmacol. Biol. Psychiatry 28 (2004) 505-516
34. Lawrence N.S., Ross T.J., and Stein E.A. Cognitive mechanisms of nicotine on visual attention. Neuron 36 (2002) 539-548
35. Leigh R.J., and Zee D.S. The neurology of eye movements (4th edition) (2006), Oxford University Press, Oxford
36. Levin E.D., McClernon F.J., and Rezvani A.H. Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 184 (2006) 523-539
37. Martin L.F., Kem W.R., and Freedman R. Alpha-7 nicotinic receptor agonists: potential new candidates for the treatment of schizophrenia. Psychopharmacology (Berl) 174 (2004) 54-64
38. Mason M.F., Norton M.I., Van Horn J.D., Wegner D.M., Grafton S.T., and Macrae C.N. Wandering minds: the default network and stimulus-independent thought. Science 315 (2007) 393-395
39. Mazoyer B., Zago L., Mellet E., Bricogne S., Etard O., Houde O., Crivello F., Joliot M., Petit L., and Tzourio-Mazoyer N. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res. Bull. 54 (2001) 287-298
40. McDowell J.E., Brown G.G., Paulus M., Martinez A., Stewart S.E., Dubowitz D.J., and Braff D.L. Neural correlates of refixation saccades and antisaccades in normal and schizophrenia subjects. Biol. Psychiatry 51 (2002) 216-223
41. McNamee R.L., Dunfee K.L., Luna B., Clark D.B., Eddy W.F., and Tarter R.E. Brain activation, response inhibition, and increased risk for substance use disorder. Alcohol Clin. Exp. Res. 32 (2008) 405-413
42. Moon S.Y., Barton J.J., Mikulski S., Polli F.E., Cain M.S., Vangel M., Hamalainen M.S., and Manoach D.S. Where left becomes right: a magnetoencephalographic study of sensorimotor transformation for antisaccades. Neuroimage 36 (2007) 1313-1323
43. Mort D.J., Perry R.J., Mannan S.K., Hodgson T.L., Anderson E., Quest R., McRobbie D., McBride A., Husain M., and Kennard C. Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage 18 (2003) 231-246
44. Newhouse P.A., Potter A., and Levin E.D. Nicotinic system involvement in Alzheimer's and Parkinson's diseases. Implications for therapeutics. Drugs Aging 11 (1997) 206-228
45. Newhouse P., Singh A., and Potter A. Nicotine and nicotinic receptor involvement in neuropsychiatric disorders. Curr. Top. Med. Chem. 4 (2004) 267-282
46. O'Driscoll G.A., Alpert N.M., Matthysse S.W., Levy D.L., Rauch S.L., and Holzman P.S. Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 925-929
47. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 (1971) 97-113
48. Perkins K.A. Baseline-dependency of nicotine effects: a review. Behav. Pharmacol. 10 (1999) 597-615
49. Postma P., Gray J.A., Sharma T., Geyer M., Mehrotra R., Das M., Zachariah E., Hines M., Williams S.C., and Kumari V. A behavioural and functional neuroimaging investigation into the effects of nicotine on sensorimotor gating in healthy subjects and persons with schizophrenia. Psychopharmacology (Berl) 184 (2006) 589-599
50. Powell J., Dawkins L., and Davis R.E. Smoking, reward responsiveness, and response inhibition: tests of an incentive motivational model. Biol. Psychiatry 51 (2002) 151-163
51. Raemaekers M., Ramsey N.F., Vink M., van den Heuvel M.P., and Kahn R.S. Brain activation during antisaccades in unaffected relatives of schizophrenic patients. Biol. Psychiatry 59 (2006) 530-535
52. Raemaekers M., Vink M., Zandbelt B., van Wezel R.J., Kahn R.S., and Ramsey N.F. Test-retest reliability of fMRI activation during prosaccades and antisaccades. Neuroimage 36 (2007) 532-542
53. Reuter B., and Kathmann N. Using saccade tasks as a tool to analyze executive dysfunctions in schizophrenia. Acta Psychol. (Amst) 115 (2004) 255-269
54. Russell M.A., Jarvis M.J., Jones G., and Feyerabend C. Non-smokers show acute tolerance to subcutaneous nicotine. Psychopharmacology (Berl) 102 (1990) 56-58
55. Rycroft N., Hutton S.B., and Rusted J.M. The antisaccade task as an index of sustained goal activation in working memory: modulation by nicotine. Psychopharmacology (Berl) 188 (2006) 521-529
56. Rycroft N., Hutton S.B., Clowry O., Groomsbridge C., Sierakowski A., and Rusted J.M. Non-cholinergic modulation of antisaccade performance: a modafinil-nicotine comparison. Psychopharmacology (Berl) 195 (2007) 245-253
57. Shadmehr R., and Holcomb H.H. Neural correlates of motor memory consolidation. Science 277 (1997) 821-825
58. Shrout P., and Fleiss J. Intraclass correlations: uses in assessing rater reliability. Psychol. Bull. 86 (1979) 420-428
59. Smith G.S., Koppel J., and Goldberg S. Applications of neuroreceptor imaging to psychiatry research. Psychopharmacol. Bull. 37 (2003) 26-65
60. Stein E.A., Pankiewicz J., Harsch H.H., Cho J.K., Fuller S.A., Hoffmann R.G., Hawkins M., Rao S.M., Bandettini P.A., and Bloom A.S. Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am. J. Psychiatry 155 (1998) 1009-1015
61. Sweeney J.A., Mintun M.A., Kwee S., Wiseman M.B., Brown D.L., Rosenberg D.R., and Carl J.R. Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J. Neurophysiol. 75 (1996) 454-468
62. Talairach J., and Tournoux P. Co-planar stereotaxic atlas of the human brain (1988), Thieme Medical Publishers, New York
63. Thaker G.K., Ellsberry R., Moran M., Lahti A., and Tamminga C. Tobacco smoking increases square-wave jerks during pursuit eye movements. Biol. Psychiatry 29 (1991) 82-88
64. Thiel C.M., Zilles K., and Fink G.R. Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology 30 (2005) 810-820
65. Tu P.C., Yang T.H., Kuo W.J., Hsieh J.C., and Su T.P. Neural correlates of antisaccade deficits in schizophrenia, an fMRI study. J. Psychiatr. Res. 40 (2006) 606-612
66. Wise R.G., and Tracey I. The role of fMRI in drug discovery. J. Magn. Reson. Imaging 23 (2006) 862-876