The impact of "physiological correction" on functional connectivity analysis of pharmacological resting state fMRI

NeuroImage

Volumn 65, Issue , 2013, Pages 499-510

  Khalili Mahani, Najmeh ^a,b   Chang, Catie ^c   van Osch, Matthias J ^b   Veer, Ilya M ^a,b   van Buchem, Mark A ^a,b   Dahan, Albert ^b   Beckmann, Christian F ^d,e   van Gerven, Joop M A ^b,f   Rombouts, Serge A R B ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF TWENTE   (Netherlands)

^f CENTRE FOR HUMAN DRUG RESEARCH   (Netherlands)

Author keywords

Drug research; Dual regression; Functional connectivity; Heart rate; Physiological noise; Respiration; Resting state fMRI

Indexed keywords

ALCOHOL; MORPHINE;

ADULT; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BOLD SIGNAL; BRAIN REGION; BRAIN SIZE; BREATHING PATTERN; CEREBELLUM; CINGULATE GYRUS; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEART HEMODYNAMICS; HEART RATE VARIABILITY; HUMAN; HUMAN EXPERIMENT; INSULA; LUNG HEMODYNAMICS; MALE; NEUROIMAGING; NEUROMODULATION; NEUROPHARMACOLOGY; NORMAL HUMAN; PRECUNEUS; PRIORITY JOURNAL; STEADY STATE; THALAMUS; VENTROMEDIAL PREFRONTAL CORTEX;

ADOLESCENT; ADULT; ARTIFACTS; BRAIN; BRAIN MAPPING; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOUBLE-BLIND METHOD; ETHANOL; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MORPHINE; NARCOTICS; NEURAL PATHWAYS; RESPIRATION; REST; YOUNG ADULT;

EID: 84868533086     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.09.044     Document Type: Article

References (55)

1. 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.
2. Birn R.M. The role of physiological noise in resting-state functional connectivity. Neuroimage 2012.
3. Birn R.M., Diamond J.B., Smith M.A., Bandettini P.A. Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 2006, 31:1536-1548.
4. Birn R.M., Murphy K., Bandettini P.A. The effect of respiration variations on independent component analysis results of resting state functional connectivity. Hum. Brain Mapp. 2008, 29:740-750.
5. Brooks J.C., Beckmann C.F., Miller K.L., Wise R.G., Porro C.A., Tracey I., Jenkinson M. Physiological noise modelling for spinal functional magnetic resonance imaging studies. Neuroimage 2008, 39:680-692.
6. Brosch J.R., Talavage T.M., Ulmer J.L., Nyenhuis J.A. Simulation of human respiration in fMRI with a mechanical model. IEEE Trans. Biomed. Eng. 2002, 49:700-707.
7. Bulte D.P., Kelly M., Germuska M., Xie J., Chappell M.A., Okell T.W., Bright M.G., Jezzard P. Quantitative measurement of cerebral physiology using respiratory-calibrated MRI. Neuroimage 2012, 60:582-591.
8. Chang C., Glover G.H. Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. Neuroimage 2009, 47:1448-1459.
9. Chang C., Glover G.H. Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI. Neuroimage 2009, 47:1381-1393.
10. Chang C., Cunningham J.P., Glover G.H. Influence of heart rate on the BOLD signal: the cardiac response function. Neuroimage 2009, 44:857-869.
11. Critchley H.D. Neural mechanisms of autonomic, affective, and cognitive integration. J. Comp. Neurol. 2005, 493:154-166.
12. Dagli M.S., Ingeholm J.E., Haxby J.V. Localization of cardiac-induced signal change in fMRI. Neuroimage 1999, 9:407-415.
13. Deckers R.H., van Gelderen P., Ries M., Barret O., Duyn J.H., Ikonomidou V.N., Fukunaga M., Glover G.H., de Zwart J.A. An adaptive filter for suppression of cardiac and respiratory noise in MRI time series data. Neuroimage 2006, 33:1072-1081.
14. Evans K.C., Shea S.A., Saykin A.J. Functional MRI localisation of central nervous system regions associated with volitional inspiration in humans. J. Physiol. 1999, 520(Pt 2):383-392.
15. Frank L.R., Buxton R.B., Wong E.C. Estimation of respiration-induced noise fluctuations from undersampled multislice fMRI data. Magn. Reson. Med. 2001, 45:635-644.
16. Glover G.H., Pauly J.M. Projection reconstruction techniques for reduction of motion effects in MRI. Magn. Reson. Med. 1992, 28:275-289.
17. Glover G.H., Li T.Q., Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000, 44:162-167.
18. Gray M.A., Minati L., Harrison N.A., Gianaros P.J., Napadow V., Critchley H.D. Physiological recordings: basic concepts and implementation during functional magnetic resonance imaging. Neuroimage 2009, 47:1105-1115.
19. Harper R.M., Gozal D., Bandler R., Spriggs D., Lee J., Alger J. Regional brain activation in humans during respiratory and blood pressure challenges. Clin. Exp. Pharmacol. Physiol. 1998, 25:483-486.
20. Harvey A.K., Pattinson K.T., Brooks J.C., Mayhew S.D., Jenkinson M., Wise R.G. Brainstem functional magnetic resonance imaging: disentangling signal from physiological noise. J. Magn. Reson. Imaging 2008, 28:1337-1344.
21. Horovitz S.G., Braun A.R., Carr W.S., Picchioni D., Balkin T.J., Fukunaga M., Duyn J.H. Decoupling of the brain's default mode network during deep sleep. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11376-11381.
22. Iacovella V., Hasson U. The relationship between BOLD signal and autonomic nervous system functions: implications for processing of "physiological noise". Magn. Reson. Imaging 2011, 29:1338-1345.
23. Jo H.J., Saad Z.S., Simmons W.K., Milbury L.A., Cox R.W. Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage 2010, 52:571-582.
24. Kastrup A., Li T.Q., Glover G.H., Moseley M.E. Cerebral blood flow-related signal changes during breath-holding. AJNR Am. J. Neuroradiol. 1999, 20:1233-1238.
25. Khalili-Mahani N., van Osch M.J., Baerends E., Soeter R.P., de Kam M., Zoethout R.W., Dahan A., van Buchem M.A., van Gerven J.M., Rombouts S.A. Pseudocontinuous arterial spin labeling reveals dissociable effects of morphine and alcohol on regional cerebral blood flow. J. Cereb. Blood Flow Metab. 2011, 31:1321-1333.
26. Khalili-Mahani N., Zoethout R.M., Beckmann C.F., Baerends E., de Kam M.L., Soeter R.P., Dahan A., van Buchem M.A., van Gerven J.M., Rombouts S.A. Effects of morphine and alcohol on functional brain connectivity during "resting state": a placebo-controlled crossover study in healthy young men. Hum. Brain Mapp. 2012, 33:1003-1018.
27. Kong Y., Jenkinson M., Andersson J., Tracey I., Brooks J.C. Assessment of physiological noise modelling methods for functional imaging of the spinal cord. Neuroimage 2012, 60:1538-1549.
28. Lee J., Santos J.M., Conolly S.M., Miller K.L., Hargreaves B.A., Pauly J.M. Respiration-induced B0 field fluctuation compensation in balanced SSFP: real-time approach for transition-band SSFP fMRI. Magn. Reson. Med. 2006, 55:1197-1201.
29. Liang K.Y., Zeger S.L. Longitudinal data-analysis using generalized linear-models. Biometrika 1986, 73:13-22.
30. Luchtmann M., Jachau K., Tempelmann C., Bernarding J. Alcohol induced region-dependent alterations of hemodynamic response: implications for the statistical interpretation of pharmacological fMRI studies. Exp. Brain Res. 2010, 204:1-10.
31. Lund T.E., Madsen K.H., Sidaros K., Luo W.L., Nichols T.E. Non-white noise in fMRI: does modelling have an impact?. Neuroimage 2006, 29:54-66.
32. Luo F., Schmidt K.F., Fox G.B., Ferris C.F. Differential responses in CBF and CBV to cocaine as measured by fMRI: implications for pharmacological MRI signals derived oxygen metabolism assessment. J. Psychiatr. Res. 2009, 43:1018-1024.
33. Madjar C., Gauthier C.J., Bellec P., Birn R.M., Brooks J.C., Hoge R.D. Task-related BOLD responses and resting-state functional connectivity during physiological clamping of end-tidal CO(2). Neuroimage 2012, 61:41-49.
34. McKay L.C., Adams L., Frackowiak R.S., Corfield D.R. A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging. Neuroimage 2008, 40:1824-1832.
35. McKay L.C., Critchley H.D., Murphy K., Frackowiak R.S., Corfield D.R. Sub-cortical and brainstem sites associated with chemo-stimulated increases in ventilation in humans. Neuroimage 2010, 49:2526-2535.
36. Murphy K., Harris A.D., Wise R.G. Robustly measuring vascular reactivity differences with breath-hold: normalising stimulus-evoked and resting state BOLD fMRI data. Neuroimage 2011, 54:369-379.
37. Napadow V., Dhond R., Conti G., Makris N., Brown E.N., Barbieri R. Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage 2008, 42:169-177.
38. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
39. Noll D.C., Genovese C.R., Vazquez A.L., O'Brien J.L., Eddy W.F. Evaluation of respiratory artifact correction techniques in multishot spiral functional MRI using receiver operator characteristic analyses. Magn. Reson. Med. 1998, 40:633-639.
40. Noth U., Kotajima F., Deichmann R., Turner R., Corfield D.R. Mapping of the cerebral vascular response to hypoxia and hypercapnia using quantitative perfusion MRI at 3 T. NMR Biomed. 2008, 21:464-472.
41. Pattinson K.T., Governo R.J., MacIntosh B.J., Russell E.C., Corfield D.R., Tracey I., Wise R.G. Opioids depress cortical centers responsible for the volitional control of respiration. J. Neurosci. 2009, 29:8177-8186.
42. Pattinson K.T., Mitsis G.D., Harvey A.K., Jbabdi S., Dirckx S., Mayhew S.D., Rogers R., Tracey I., Wise R.G. Determination of the human brainstem respiratory control network and its cortical connections in vivo using functional and structural imaging. Neuroimage 2009, 44:295-305.
43. Perthen J.E., Lansing A.E., Liau J., Liu T.T., Buxton R.B. Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: a calibrated BOLD fMRI study. Neuroimage 2008, 40:237-247.
44. Pfeuffer J., Van de Moortele P.F., Ugurbil K., Hu X., Glover G.H. Correction of physiologically induced global off-resonance effects in dynamic echo-planar and spiral functional imaging. Magn. Reson. Med. 2002, 47:344-353.
45. Sarton E., Olofsen E., Romberg R., den Hartigh J., Kest B., Nieuwenhuijs D., Burm A., Teppema L., Dahan A. Sex differences in morphine analgesia: an experimental study in healthy volunteers. Anesthesiology 2000, 93:1245-1254. (discussion 1246A).
46. Shmueli K., van Gelderen P., de Zwart J.A., Horovitz S.G., Fukunaga M., Jansma J.M., Duyn J.H. Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage 2007, 38:306-320.
47. Starck T., Remes J., Nikkinen J., Tervonen O., Kiviniemi V. Correction of low-frequency physiological noise from the resting state BOLD fMRI-effect on ICA default mode analysis at 1.5T. J. Neurosci. Methods 2010, 186:179-185.
48. Teichert T., Grinband J., Hirsch J., Ferrera V.P. Effects of heartbeat and respiration on macaque fMRI: implications for functional connectivity. Neuropsychologia 2010, 48:1886-1894.
49. van Buuren M., Gladwin T.E., Zandbelt B.B., van den Heuvel M., Ramsey N.F., Kahn R.S., Vink M. Cardiorespiratory effects on default-mode network activity as measured with fMRI. Hum. Brain Mapp. 2009, 30:3031-3042.
50. van Buuren M., Gladwin T.E., Zandbelt B.B., Kahn R.S., Vink M. Reduced functional coupling in the default-mode network during self-referential processing. Hum. Brain Mapp. 2010, 31:1117-1127.
51. Van de Moortele P.F., Pfeuffer J., Glover G.H., Ugurbil K., Hu X. Respiration-induced B0 fluctuations and their spatial distribution in the human brain at 7Tesla. Magn. Reson. Med. 2002, 47:888-895.
52. Wise R.G., Ide K., Poulin M.J., Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004, 21:1652-1664.
53. Zeger S.L., Liang K.Y., Albert P.S. Models for longitudinal data - a generalized estimating equation approach. Biometrics 1988, 44:1049-1060.
54. Zoethout R.W., van Gerven J.M., Dumont G.J., Paltansing S., van Burgel N.D., van der Linden M., Dahan A., Cohen A.F., Schoemaker R.C. A comparative study of two methods for attaining constant alcohol levels. Br. J. Clin. Pharmacol. 2008, 66:674-681.
55. 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.