The BOLD response and the gamma oscillations respond differently than evoked potentials: an interleaved EEG-fMRI study

BMC Neuroscience

Daniel Gounot²  Hélène Otzenberger²  Jack R Foucher¹ 

[1] Clinique Psychiatrique – INSERM U405, Hôpitaux Universitaires – BP 406 – 67091 Strasbourg Cedex – France;UMR 7004 – CNRS/ULP – Institut de Physique Biologique, 4 rue Kirschleger – 67085 Strasbourg Cedex – France

关键词: top-down;    bottom-up;    attention;    frontal lobe;    no-go;    3-stimulus paradigm;    P3b;    P3a;    temporal-parietal junction;    Novels;    oddball;    P300;    synchrony;   

Others  :  1223212
DOI  :  10.1186/1471-2202-4-22

 received in 2003-06-03, accepted in 2003-09-19,  发布年份 2003

【 摘 要 】

Background

The integration of EEG and fMRI is attractive because of their complementary precision regarding time and space. But the relationship between the indirect hemodynamic fMRI signal and the more direct EEG signal is uncertain. Event-related EEG responses can be analyzed in two different ways, reflecting two different kinds of brain activity: evoked, i.e. phase-locked to the stimulus, such as evoked potentials, or induced, i.e. non phase-locked to the stimulus such as event-related oscillations. In order to determine which kind of EEG activity was more closely related with fMRI, EEG and fMRI signals were acquired together, while subjects were presented with two kinds of rare events intermingled with frequent distractors. Target events had to be signaled by pressing a button and Novel events had to be ignored.

Results

Both Targets and Novels triggered a P300, of larger amplitude in the Novel condition. On the opposite, the fMRI BOLD response was stronger in the Target condition. EEG event-related oscillations in the gamma band (32–38 Hz) reacted in a way similar to the BOLD response.

Conclusions

The reasons for such opposite differential reactivity between oscillations / fMRI on the one hand, and evoked potentials on the other, are discussed in the paper. Those results provide further arguments for a closer relationship between fast oscillations and the BOLD signal, than between evoked potentials and the BOLD signal.

【 授权许可】

   
2003 Foucher et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

【 图 表 】

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【 参考文献 】

• [1]Aine CJ: A conceptual overview and critique of functional neuroimaging techniques in humans: I. MRI/FMRI and PET. Crit Rev Neurobiol 1995, 9:229-309.
• [2]Mathiesen C, Caesar K, Akgoren N, Lauritzen M: Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J Physiol 1998, 512:555-566.
• [3]Mathiesen C, Caesar K, Lauritzen M: Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis. J Physiol 2000, 523(Pt 1):235-246.
• [4]Matsuura T, Kanno I: Quantitative and temporal relationship between local cerebral blood flow and neuronal activation induced by somatosensory stimulation in rats. Neurosci Res 2001, 40:281-290.
• [5]Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A: Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
• [6]Polich J: Neuropsychology of P3a and P3b: a theoretical overview. In In Advances in electrophysiology in clinical practice and research. Edited by Arikan K, Moore N. Wheaton: Kjellberg; 2002.
• [7]Lopes da Silva FH: Event-related potentials: Methodology and quantification. In In Electroencephalography, basic principles, clinical applications and related fields. Edited by Niedermeyer E, Lopes da Silva F. Williams & Wilkins; 1999:947-957.
• [8]Soltani M, Knight RT: Neural origins of the P300. Crit Rev Neurobiol 2000, 14:199-224.
• [9]Halgren E, Baudena P, Clarke JM, Heit G, Liegeois C, Chauvel P, et al.: Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. Electroencephalogr Clin Neurophysiol 1995, 94:191-220.
• [10]Halgren E, Baudena P, Clarke JM, Heit G, Marinkovic K, Devaux B, et al.: Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. Electroencephalogr Clin Neurophysiol 1995, 94:229-250.
• [11]Courchesne E, Hillyard SA, Galambos R: Stimulus novelty, task relevance and the visual evoked potential in man. Electroencephalogr Clin Neurophysiol 1975, 39:131-143.
• [12]Knight RT: Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 1984, 59:9-20.
• [13]Clark VP, Fannon S, Lai S, Benson R: Paradigm-dependent modulation of event-related fMRI activity evoked by the oddball task. Hum Brain Mapp 2001, 14:116-127.
• [14]Clark VP, Fannon S, Lai S, Benson R, Bauer L: Responses to rare visual target and distractor stimuli using event-related fMRI. J Neurophysiol 2000, 83:3133-3139.
• [15]Kirino E, Belger A, Goldman-Rakic P, McCarthy G: Prefrontal activation evoked by infrequent target and novel stimuli in a visual target detection task: an event-related functional magnetic resonance imaging study. J Neurosci 2000, 20:6612-6618.
• [16]Kiehl KA, Liddle PF: An event-related functional magnetic resonance imaging study of an auditory oddball task in schizophrenia. Schizophr Res 2001, 48:159-171.
• [17]Bonmassar G, Anami K, Ives J, Belliveau JW: Visual evoked potential (VEP) measured by simultaneous 64-channel EEG and 3T fMRI. Neuroreport 1999, 10:1893-1897.
• [18]Kruggel F, Wiggins CJ, Herrmann CS, von Cramon DY: Recording of the event-related potentials during functional MRI at 3.0 Tesla field strength. Magn Reson Med 2000, 44:277-282.
• [19]Varela FJ, Lachaux JP, Rodriguez E, Martinerie J: The brainweb : phase synchronization and large-scale integration. Nature Reviews in Neuroscience 2001, 2:229-239.
• [20]Tallon-Baudry C, Bertrand O: Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 1999, 3:151-162.
• [21]Duzel E, Habib R, Schott B, Schoenfeld A, Lobaugh N, McIntosh AR, et al.: A multivariate, spatiotemporal analysis of electromagnetic time-frequency data of recognition memory. Neuroimage 2003, 18:185-197.
• [22]Marshall L, Molle M, Bartsch P: Event-related gamma band activity during passive and active oddball tasks. Neuroreport 1996, 7:1517-1520.
• [23]Fell J, Hinrichs H, Roschke J: Time course of human 40 Hz EEG activity accompanying P3 responses in an auditory oddball paradigm. Neurosci Lett 1997, 235:121-124.
• [24]Haig AR, De PV, Gordon E: Peak gamma latency correlated with reaction time in a conventional oddball paradigm. Clin Neurophysiol 1999, 110:158-165.
• [25]Gurtubay IG, Alegre M, Labarga A, Malanda A, Iriarte J, Artieda J: Gamma band activity in an auditory oddball paradigm studied with the wavelet transform. Clin Neurophysiol 2001, 112:1219-1228.
• [26]Reilly EL: EEG recording and operation of the apparatus. In In Electroencephalography, basic principles, clinical applications and related fields. Edited by Niedermeyer E, Lopes da Silva F. Williams & Wilkins; 1999:122-142.
• [27]Schomer DL, Bonmassar G, Lazeyras F, Seeck M, Blum A, Anami K, et al.: EEG-Linked functional magnetic resonance imaging in epilepsy and cognitive neurophysiology. J Clin Neurophysiol 2000, 17:43-58.
• [28]Demiralp T, Ademoglu A, Comerchero M, Polich J: Wavelet analysis of P3a and P3b. Brain Topogr 2001, 13:251-267.
• [29]Menon V, Ford JM, Lim KO, Glover GH, Pfefferbaum A: Combined event-related fMRI and EEG evidence for temporal-parietal cortex activation during target detection. Neuroreport 1997, 8:3029-3037.
• [30]McCarthy G, Luby M, Gore J, Goldman-Rakic P: Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. J Neurophysiol 1997, 77:1630-1634.
• [31]Yoshiura T, Zhong J, Shibata DK, Kwok WE, Shrier DA, Numaguchi Y: Functional MRI study of auditory and visual oddball tasks. Neuroreport 1999, 10:1683-1688.
• [32]Stevens AA, Skudlarski P, Gatenby JC, Gore JC: Event-related fMRI of auditory and visual oddball tasks. Magn Reson Imaging 2000, 18:495-502.
• [33]Downar J, Crawley AP, Mikulis DJ, Davis KD: A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J Neurophysiol 2002, 87:615-620.
• [34]Downar J, Crawley AP, Mikulis DJ, Davis KD: A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 2000, 3:277-283.
• [35]Downar J, Crawley AP, Mikulis DJ, Davis KD: The effect of task relevance on the cortical response to changes in visual and auditory stimuli: an event-related fMRI study. Neuroimage 2001, 14:1256-1267.
• [36]Corbetta M, Shulman GL: Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 2002, 3:201-215.
• [37]Liddle PF, Kiehl KA, Smith AM: Event-related fMRI study of response inhibition. Hum Brain Mapp 2001, 12:100-109.
• [38]Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y: Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 1999, 122(Pt 5):981-991.
• [39]Konishi S, Nakajima K, Uchida I, Sekihara K, Miyashita Y: No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. Eur J Neurosci 1998, 10:1209-1213.
• [40]Fallgatter AJ, Brandeis D, Strik WK: A robust assessment of the NoGo-anteriorisation of P300 microstates in a cued Continuous Performance Test. Brain Topogr 1997, 9:295-302.
• [41]Sasaki K, Gemba H, Nambu A, Matsuzaki R: No-go activity in the frontal association cortex of human subjects. Neurosci Res 1993, 18:249-252.
• [42]Fallgatter AJ, Esienack SS, Neuhauser B, Aranda D, Scheuerpflug P, Herrmann MJ: Stability of late event-related potentials: topographical descriptors of motor control compared with the P300 amplitude. Brain Topogr 2000, 12:255-261.
• [43]Bisiach E, Mini M, Sterzi R, Vallar G: Hemispheric lateralization of the decisional stage in choice reaction times to visual unstructured stimuli. Cortex 1982, 18:191-197.
• [44]Vallar G, Bisiach E, Cerizza M, Rusconi ML: The role of the left hemisphere in decision-making. Cortex 1988, 24:399-410.
• [45]Konishi S, Wheeler ME, Donaldson DI, Buckner RL: Neural correlates of episodic retrieval success. Neuroimage 2000, 12:276-286.
• [46]McDermott KB, Jones TC, Petersen SE, Lageman SK, Roediger HL III: Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: an event-related fMRI study. J Cogn Neurosci 2000, 12:965-976.
• [47]Donaldson DI, Petersen SE, Ollinger JM, Buckner RL: Dissociating state and item components of recognition memory using fMRI. Neuroimage 2001, 13:129-142.
• [48]Logothetis NK: The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 2002, 357:1003-1037.
• [49]Speckmann EJ, Elger CE: Introduction to the neurophysiological basis of the EEG and DC potentials. In In Electroencephalography, basic principles, clinical applications and related fields. Edited by Niedermeyer E, Lopes da Silva F. Williams & Wilkins; 1999:15-27.
• [50]Baillet S, Mosher JC, Leahy RM: Electromagnetic brain mapping. IEEE Signal Proc Mag 2001, 18:14-30.
• [51]Traub RD, Whittington MA, Colling SB, Buzsaki G, Jefferys JG: Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 1996, 493(Pt 2):471-484.
• [52]Traub RD, Jefferys JG, Whittington MA: Fast oscillations in cortical cicuits. Cambridge MA: MIT Press; 1999.
• [53]Chelazzi L, Duncan J, Miller EK, Desimone R: Responses of neurons in inferior temporal cortex during memory-guided visual search. J Neurophysiol 1998, 80:2918-2940.
• [54]Jagadeesh B, Chelazzi L, Mishkin M, Desimone R: Learning increases stimulus salience in anterior inferior temporal cortex of the macaque. J Neurophysiol 2001, 86:290-303.
• [55]Engel AK, Fries P, Singer W: Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2001, 2:704-716.
• [56]Fries P, Reynolds JH, Rorie AE, Desimone R: Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
• [57]Goldman RI, Stern JM, Engel J Jr, Cohen MS: Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport 2002, 13:2487-2492.
• [58]Pfurtscheller G, Lopes da Silva FH: Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 1999, 110:1842-1857.
• [59]Tass PA: Phase resetting in medecine an biology. Spinger-Verlag; 1999.
• [60]Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, et al.: Dynamic brain sources of visual evoked responses. Science 2002, 295:690-694.
• [61]Pallier C, Dupoux E, Jeannin X: Expe: an expandable programming language for on-line psychological experiments. Behavior Research Methods, Instruments and Computers 1997, 29:322-327.
• [62]Friston KJ, Zarahn E, Josephs O, Henson RN, Dale AM: Stochastic designs in event-related fMRI. Neuroimage 1999, 10:607-619.
• [63]Polich J: P300 in clinical applications. In In Electroencephalography : basic principles, clinical applications and related fields. Edited by Niedermeyer E, Lopes da Silva F. Baltimore: Williams & Wilkins; 1999:1073-1091.
• [64]Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frackowiak RSJ: Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995, 2:189-210.
• [65]Josephs O, Henson RN: Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos Trans R Soc Lond B Biol Sci 1999, 354:1215-1228.
• [66]Friston KJ, Holmes AP, Worsley KJ: How many subjects constitute a study? Neuroimage 1999, 10:1-5.
• [67]Friston KJ, Holmes AP, Price CJ, Buchel C, Worsley KJ: Multisubject fMRI studies and conjunction analyses. Neuroimage 1999, 10:385-396.
• [68]xx x: American Electroencephalographic Society guidelines for standard electrode position nomenclature. J Clin Neurophysiol 1991, 8:200-202.
• [69]Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L: Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1998, 8:229-239.
• [70]Hoffmann A, Jager L, Werhahn KJ, Jaschke M, Noachtar S, Reiser M: Electroencephalography during functional echo-planar imaging: detection of epileptic spikes using post-processing methods. Magn Reson Med 2000, 44:791-798.
• [71]Lachaux JP, Rodriguez E, Martinerie J, Varela FJ: Measuring phase synchrony in brain signals. Hum Brain Mapp 1999, 8:194-208.
• [72]Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ: Perception's shadow: long-distance synchronization of human brain activity. Nature 1999, 397:430-433.
• [73]Le Van QM, Foucher J, Lachaux J, Rodriguez E, Lutz A, Martinerie J, et al.: Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J Neurosci Methods 2001, 111:83-98.
• [74]Nichols TE, Holmes AP: Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002, 15:1-25.