EEG-informed fMRI analysis during a hand grip task: Estimating the relationship between EEG rhythms and the BOLD signal

Frontiers in Human Neuroscience

Volumn 8, Issue 1 APR, 2014, Pages

  Sclocco, Roberta ^a   Tana, Maria G ^a,b   Visani, Elisa ^c   Gilioli, Isabella ^c   Panzica, Ferruccio ^c   Franceschetti, Silvana ^c   Cerutti, Sergio ^a   Bianchi, Anna M ^a  

^a POLITECNICO DI MILANO   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Alpha rhythm; Beta rhythm; BOLD; EEG fMRI; GLM; Motor task; Neural correlates

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND GRIP; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; MOTOR PERFORMANCE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; STIMULUS;

EID: 84897410857     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00186     Document Type: Article

References (52)

1. Allen, P. J., Josephs, O., and Turner, R. (2000). A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12, 230-239. doi: 10.1006/nimg.2000.0599
2. Babiloni, F., Cincotti, F., Babiloni, C., Carducci, F., Mattia, D., Astolfi, L., et al. (2005). Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function. Neuroimage 24, 118-131. doi: 10.1016/j.neuroimage.2004.09.036
3. Büchel, C., and Friston, K. (1997). Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. Cereb. Cortex 7, 768-778. doi: 10.1093/cercor/7.8.768
4. Cooreman, C., Sclocco, R., Tana, M. G., Vanderperren, K., Visani, E., Panzica, F., et al. (2011). "BOLD correlates of Alpha and Beta EEG-rhythm during a motor task, " in Neural Engineering (NER), 2011 5th International IEEE/EMBS Conference on (Cancun), 25-28. doi: 10.1109/NER.2011.5910481
5. Coull, J. T. (1998). Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology. Prog. Neurobiol. 55, 343-361. doi: 10.1016/S0301-0082(98)00011-2
6. Crone, N. E., Miglioretti, D. L., Gordon, B., and Lesser, R. P. (1998a). Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121, 2301-2315. doi: 10.1093/brain/121.12.2301
7. Crone, N. E., Miglioretti, D. L., Gordon, B., Sieracki, J. M., Wilson, M. T., Uematsu, S., et al. (1998b). Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 121, 2271-2299. doi: 10.1093/brain/121.12.2271
8. Dale, A. M., Liu, A. K., Fischl, B. R., Buckner, R. L., Belliveau, J. W., Lewine, J. D., et al. (2000). Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 26, 55-67. doi: 10.1016/S0896-6273(00)81138-1
9. Dosenbach, N. U., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A., et al. (2007). Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U.S.A. 104, 11073-11078. doi: 10.1073/pnas.0704320104
10. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25, 1325-1335. doi: 10.1016/j.neuroimage.2004.12.034
11. Feige, B., Scheffler, K., Esposito, F., Di Salle, F., Hennig, J., and Seifritz, E. (2005). Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. J. Neurophysiol. 93, 2864-2872. doi: 10.1152/jn.00721.2004
12. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. P., Frith, C. D., and Frackowiak, R. S. J. (1994). Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 210. doi: 10.1002/hbm.460010306
13. Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S. J., and Turner, R. (1996). Movement-related effects in fMRI time-series. Magn. Reson. Med. 35, 346-355. doi: 10.1002/mrm.1910350312
14. Gastaut, H. (1952). Electrocorticographic study of the reactivity of rolandic rhythm. Rev. Neurol. 87, 176-182.
15. Goense, J. B. M., and Logothetis, N. K. (2008). Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 18, 631-640. doi: 10.1016/j.cub.2008.03.054
16. He, B., and Liu, Z. (2008). Multimodal functional neuroimaging: integrating functional MRI and EEG/MEG. IEEE Rev. Biomed. Eng. 1, 23-40. doi: 10.1109/RBME.2008.2008233
17. Henson, R., and Friston, K. J. (2007). "Convolution models for fMRI, " in Statistical Parametric Mapping: the Analysis of Functional Brain Images Anonymous (Amsterdam: Elsevier), 178-192.
18. Hjorth, B. (1975). An on-line transformation of EEG scalp potentials into orthogonal source derivations. Electroencephalogr. Clin. Neurophysiol. 39, 526-530. doi: 10.1016/0013-4694(75)90056-5
19. Horovitz, S. G., Fukunaga, M., de Zwart, J. A., van Gelderen, P., Fulton, S. C., Balkin, T. J., et al. (2008). Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum. Brain Mapp. 29, 671-682. doi: 10.1002/hbm.20428
20. Josephs, O., Turner, R., and Friston, K. (1997). Event-related fMRI. Hum. Brain Mapp. 5, 243-248. doi: 10.1002/(SICI)1097-0193(1997)5:4<243::AID-HBM7>3.0.CO;2-3
21. Kilner, J. M., Mattout, J., Henson, R., and Friston, K. J. (2005). Hemodynamic correlates of EEG: a heuristic. Neuroimage 28, 280-286. doi: 10.1016/j.neuroimage.2005.06.008
22. Laufs, H., Kleinschmidt, A., Beyerle, A., Eger, E., Salek-Haddadi, A., Preibisch, C., et al. (2003). EEG-correlated fMRI of human alpha activity. Neuroimage 19, 1463-1476. doi: 10.1016/S1053-8119(03)00286-6
23. Liu, Z., Ding, L., and He, B. (2006). Integration of EEG/MEG with MRI and fMRI. IEEE Eng. Med. Biol. Mag. 25, 46-53. doi: 10.1109/MEMB.2006.1657787
24. Liu, A. K., Belliveau, J. W., and Dale, A. M. (1998). Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. Proc. Natl. Acad. Sci. U.S.A. 95, 8945-8950. doi: 10.1073/pnas.95.15.8945
25. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 157. doi: 10.1038/35084005
26. MacKay, W. A., and Crammond, D. J. (1987). Neuronal correlates in posterior parietal lobe of the expectation of events. Behav. Brain Res. 24, 167-179. doi: 10.1016/0166-4328(87)90055-6
27. Mantini, D., Perrucci, M. G., Del Gratta, C., Romani, G. L., and Corbetta, M. (2007). Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U.S.A. 104, 13170-13175. doi: 10.1073/pnas.0700668104
28. Marsden, J., Werhahn, K., Ashby, P., Rothwell, J., Noachtar, S., and Brown, P. (2000). Organization of cortical activities related to movement in humans. J. Neurosci. 20, 2307-2314.
29. Moosmann, M., Ritter, P., Krastel, I., Brink, A., Thees, S., Blankenburg, F., et al. (2003). Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. Neuroimage 20, 145-158. doi: 10.1016/S1053-8119(03)00344-6
30. Niazy, R. K., Beckmann, C. F., Iannetti, G. D., Brady, J. M., and Smith, S. M. (2005). Removal of FMRI environment artifacts from EEG data using optimal basis sets. Neuroimage 28, 720-737. doi: 10.1016/j.neuroimage.2005.06.067
31. Ohara, S., Mima, T., Baba, K., Ikeda, A., Kunieda, T., Matsumoto, R., et al. (2001). Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements. J. Neurosci. 21, 9377-9386.
32. Papakostopoulos, D., Crow, H. J., and Newton, P. (1980). "Spatiotemporal characteristics of intrinsic evoked and event-related potentials in the human cortex, " in Rhythmic EEG Activities and Cortical Functioning, eds G. Pfurtscheller, F. H. Lopes da Silva, and H. Petsche (Amsterdam: Elsevier), 179-200.
33. Parkes, L. M., Bastiaansen, M. C. M., and Norris, D. G. (2006). Combining EEG and fMRI to investigate the post-movement beta rebound. Neuroimage 29, 685-696. doi: 10.1016/j.neuroimage.2005.08.018
34. Pfurtscheller, G. (1981). Central beta rhythm during sensorimotor activities in man. Electroencephalogr. Clin. Neurophysiol. 51, 253-264. doi: 10.1016/0013-4694(81)90139-5
35. Pfurtscheller, G., and Lopes da Silva, F. H. (1999). Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 110, 1842-1857. doi: 10.1016/S1388-2457(99)00141-8
36. Popivanov, D., Mineva, A., and Krekule, I. (1999). EEG patterns in theta and gamma frequency range and their probable relation to human voluntary movement organization. Neurosci. Lett. 267, 5-8. doi: 10.1016/S0304-3940(99)00271-2
37. Ritter, P., Moosmann, M., and Villringer, A. (2009). Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI-BOLD signal in primary somatosensory and motor cortex. Hum. Brain Mapp. 30, 1168-1187. doi: 10.1002/hbm.20585
38. Rosa, M. J., Kilner, J., Blankenburg, F., Josephs, O., and Penny, W. (2010). Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI. Neuroimage 49, 1496-1509. doi: 10.1016/j.neuroimage.2009.09.011
39. Rushworth, M. F. S., Krams, M., and Passingham, R. E. (2001). The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J. Cogn. Neurosci. 13, 698-710. doi: 10.1162/089892901750363244
40. Rushworth, M. F. S., Nixon, P. D., Renowden, S., Wade, D. T., and Passingham, R. E. (1997). The left parietal cortex and motor attention. Neuropsychologia 35, 1261-1273. doi: 10.1016/S0028-3932(97)00050-X
41. Sadaghiani, S., Scheeringa, R., Lehongre, K., Morillon, B., Giraud, A. L., D'Esposito, M., et al. (2012). Alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network. J. Neurosci. 32, 14305-14310. doi: 10.1523/JNEUROSCI.1358-12.2012
42. Sadaghiani, S., Scheeringa, R., Lehongre, K., Morillon, B., Giraud, A. L., and Kleinschmidt, A. (2010). Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J. Neurosci. 30, 10243-10250. doi: 10.1523/JNEUROSCI.1004-10.2010
43. Salmelin, R., Hámáaláinen, M., Kajola, M., and Hari, R. (1995). Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 2, 237-243. doi: 10.1006/nimg.1995.1031
44. Salmelin, R., and Hari, R. (1994). Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 60, 537-550. doi: 10.1016/0306-4522(94)90263-1
45. Scheeringa, R., Fries, P., Petersson, K., Oostenveld, R., Grothe, I., Norris, D. G., et al. (2011). Neuronal dynamics underlying high-and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 69, 572-583. doi: 10.1016/j.neuron.2010.11.044
46. Sclocco, R., Tana, M. G., Visani, E., Gilioli, I., Panzica, F., Franceschetti, S., et al. (2012). "EEG-informed fMRI analysis during a hand grip task, " in Engineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE (San Diego, CA), 4712-4715. doi: 10.1109/EMBC.2012.6347019
47. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme Medical Publishers.
48. Tallon-Baudry, C., and Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3, 151-162. doi: 10.1016/S1364-6613(99)01299-1
49. Turak, B., Louvel, J., Buser, P., and Lamarche, M. (2001). Parieto-temporal rhythms in the 6-9 Hz band recorded in epileptic patients with depth electrodes in a self-paced movement protocol. Clin. Neurophysiol. 112, 2069-2074. doi: 10.1016/S1388-2457(01)00652-6
50. Visani, E., Agazzi, P., Canafoglia, L., Panzica, F., Ciano, C., Scaioli, V., et al. (2006). Movement-related desynchronization-synchronization (ERD/ERS) in patients with Unverricht-Lundborg disease. Neuroimage 33, 161-168. doi: 10.1016/j.neuroimage.2006.06.036
51. Visani, E., Minati, L., Canafoglia, L., Gilioli, I., Granvillano, A., Varotto, G., et al. (2011). Abnormal ERD/ERS but unaffected BOLD response in patients with Unverricht-Lundborg disease during index extension: a simultaneous EEG-fMRI study. Brain Topogr. 24, 65-77. doi: 10.1007/s10548-010-0167-5
52. Willemse, R. B., de Munck, J. C., Verbunt, J. P. A., van't Ent, D., Ris, P., Baayen, J. C., et al. (2010). Topographical organization of mu and Beta band activity associated with hand and foot movements in patients with perirolandic lesions. Open Neuroimag. J. 4, 93-99. doi: 10.2174/1874440001004010093