Chapter 4 - Electro- and Magneto-Encephalography in the Study of Emotion  pp. 107-132

Electro- and Magneto-Encephalography in the Study of Emotion

By Andreas Keil

Image View Previous Chapter Next Chapter



The conscious stream has fuzzy water in it, as well as driftwood, swimming fish, floating leaves and grass, and of course, careful scientific thinking.

– William James, Principles of Psychology

Affective neuroscience studies using electro-encephalography (EEG) or magneto-encep-halography (MEG) frequently highlight these methods’ exquisite temporal resolution for capturing the electrophysiology of emotion. Although this is already a desirable property, electrophysiological measurements have additional advantages: They are more affordable than hemodynamic imaging techniques, are widely available, and impose little if any discomfort on research participants. As a consequence, electrophysiological methods have found wide application in the cognitive and affective neurosciences. Recent years have seen exciting developments in virtually every aspect of EEG/MEG research of emotion, ranging from innovation in data-recording techniques to novel experimental paradigms and sophisticated analysis techniques. It is now possible to record from high-density sensor arrays at hundreds of extracranial locations, providing impressive spatial sampling along with high temporal accuracy. Combination of electrophysiological methods with other imaging modalities has been particularly fruitful. Modeling studies of meso- and macroscopic brain activity (i.e., activity in small and large groups of neurons) have provided a constantly improving conceptual framework for interpreting the measured signals.

Because of this rich potential for addressing pertinent questions in the affective neurosciences, human electrophysiology has been a popular avenue for studying emotion. Over the last decade, this field has seen high productivity, with increasing numbers of published research reports, now accounting for hundreds of papers per year. In fact, electrophysiological measures have been used to address questions centered on human emotional experience and behavior since their inception in the late 1920s. It is thus helpful to begin by reviewing a few key events that have shaped the present state of the field.

Büchel, C. , Coull, J. T. , & Friston, K. J. (1999). The predictive value of changes in effective connectivity for human learning. Science, 283(5407), 1538–41.
Bar-Haim, Y. , Lamy, D. , Pergamin, L. , Bakermans-Kranenburg, M. J. , & van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–24.
Bayle, D. J. , Henaff, M. A. , & Krolak-Salmon, P. (2009). Unconsciously perceived fear in peripheral vision alerts the limbic system: A MEG study. PLoS One, 4(12), e8207.
Berger, H. (1969). On the electroencephalogram of man. Electroencephalography and Clinical Neurophysiology, 28[Suppl.], 37.
Bertrand, O. , Bohorquez, J. , & Pernier, J. (1994). Time-frequency digital filtering based on an invertible wavelet transform: An application to evoked potentials. IEEE Transactions of Biomedical Engineering, 41(1), 77–88.
Blair, R. C. , & Karniski, W. (1993). An alternative method for significance testing of waveform difference potentials. Psychophysiology, 30(5), 518–24.
Borck, C. (2005). Hirnströme – Eine Kulturgeschichte der Elektroenzephalographie. Göttingen: Wallstein.
Bradley, M. M. , Hamby, S. , Low, A. , & Lang, P. J. (2007). Brain potentials in perception: Picture complexity and emotional arousal. Psychophysiology, 44(3), 364–73.
Cahn, B. R. , & Polich, J. (2006). Meditation states and traits: EEG, ERP, and neuroimaging studies. Psychology Bulletin, 132(2), 180–211.
Cohen, D. (1968). Magnetoencephalography: Evidence of magnetic fields produced by alpha-rhythm currents. Science, 161(843), 784–86.
Cohen, D. (1972). Magnetoencephalography: Detection of the brain's electrical activity with a superconducting magnetometer. Science, 175(22), 664–66.
Cohen, D. , & Cuffin, B. N. (1987). A method for combining MEG and EEG to determine the sources. Physics in Medicine and Biology, 32(1), 85–89.
Cohen, D. , & Cuffin, B. N. (1991). EEG versus MEG localization accuracy: Theory and experiment. Brain Topography, 4(2), 95–103.
Cohen, D. , Cuffin, B. N. , Yunokuchi, K. , Maniewski, R. , Purcell, C. , Cosgrove, G. R. , et al. (1990). MEG versus EEG localization test using implanted sources in the human brain. Annals of Neurology, 28(6), 811–17.
Cook, E. W. , III, & Miller, G. A. (1992). Digital filtering: Background and tutorial for psychophysiologists. Psychophysiology, 29(3), 350–67.
Cuthbert, B. N. , Schupp, H. T. , Bradley, M. , McManis, M. , & Lang, P. J. (1998). Probing affective pictures: Attended startle and tone probes. Psychophysiology, 35(3), 344–47.
Cuthbert, B. N. , Schupp, H. T. , Bradley, M. M. , Birbaumer, N. , & Lang, P. J. (2000). Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52(2), 95–111.
Davidson, R. J. (1995). Cerebral asymmetry, emotion, and affective style. In R. J. Davidson & K. Hugdahl (Eds.), Brain asymmetry (pp. 361–87). Cambridge, MA: MIT Press.
Davidson, R. J. , Pizzagalli, D. , Nitschke, J. B. , & Putnam, K. (2002). Depression: Perspectives from affective neuroscience. Annual Review of Psychology, 53, 545–74.
Delorme, A. , & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21.
Dien, J. (2010). Evaluating two-step PCA of ERP data with Geomin, Infomax, Oblimin, Promax, and Varimax rotations. Psychophysiology, 47(1), 170–83.
Ding, L. , & He, B. (2008). Sparse source imaging in electroencephalography with accurate field modeling. Human Brain Mapping, 29(9), 1053–67.
Elliott, G. , Rothenberg, T. J. , & Stock, J. (1996). Efficient tests for an autoregressive unit root. Econometrica, 64(4), 813–36.
Ferree, T. C. , Luu, P. , Russell, G. S. , & Tucker, D. M. (2001). Scalp electrode impedance, infection risk, and EEG data quality. Clinical Neurophysiology, 112(3), 536–44.
Flor, H. , Braun, C. , Elbert, T. , & Birbaumer, N. (1997). Extensive reorganization of primary somatosensory cortex in chronic back pain patients. Neuroscience Letters, 224(1), 5–8.
Foti, D. , Hajcak, G. , & Dien, J. (2009) Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. Psychophysiology, 46, 521–30.
Frund, I. , Schadow, J. , Busch, N. A. , Korner, U. , & Herrmann, C. S. (2007). Evoked gamma oscillations in human scalp EEG are test-retest reliable. Clinical Neurophysiology, 118(1), 221–27.
Galambos, R. (1992). A comparison of certain gamma-band (40 Hz) brain rhythms in cat and man. In E. Basar & T. Bullock (Eds.), Induced rhythms in the brain (pp. 103–22). Berlin: Springer.
Gianotti, L. R. , Faber, P. L. , Schuler, M. , Pascual-Marqui, R. D. , Kochi, K. , & Lehmann, D. (2008). First valence, then arousal: The temporal dynamics of brain electric activity evoked by emotional stimuli. Brain Topography, 20(3), 143–56.
Grave de Peralta, R. , Hauk, O. , & Gonzalez, S. L. (2009). The neuroelectromagnetic inverse problem and the zero dipole localization error. Computational Intelligence and Neuroscience, 659247.
Groppe, D. (2011). Mass univariate analysis of event-related brain potentials/fields I: A critical tutorial review. Psychophysiology, 48(12),1726–37.
Hämäläinen, M. , & Ilmoniemi, R. (1984). Interpreting measured magnetic fields of the brain: Estimates of current distributions. (Technical Report No. TKK-F-A559). Helsinki: Helsinki University of Technology.
Hajcak, G. , Weinberg, A. , MacNamara, A. , & Foti, D. (2011). ERPs and the study of emotion. In S. J. Luck & E. Kappenman (Eds.), Oxford handbook of event-related potential components (pp. 441–74). New York: Oxford University Press.
Haken, H. (1983). Synergetics: An introduction. Berlin: Springer.
Heim, S. , & Keil, A. (2006). Effects of classical conditioning on identification and cortical processing of speech syllables. Experimental Brain Research, 175, 411–24.
Homma, S. , Nakajima, Y. , Toma, S. , Ito, T. , & Shibata, T. (1998). Intracerebral source localization of mental process-related potentials elicited prior to mental sweating response in humans. Neuroscience Letters, 247(1), 25–28.
Ille, N. , Berg, P. , & Scherg, M. (2002). Artifact correction of the ongoing EEG using spatial filters based on artifact and brain signal topographies. Journal of Clinical Neurophysiology, 19(2), 113–24.
Johnston, V. S. , & Wang, X. T. (1991). The relationship between menstrual phase and the P3 component of ERPs. Psychophysiology, 28(4), 400–9.
Junghöfer, M. , Bradley, M. M. , Elbert, T. R. , & Lang, P. J. (2001). Fleeting images: A new look at early emotion discrimination. Psychophysiology, 38(2), 175–78.
Junghöfer, M. , Elbert, T. , Tucker, D. M. , & Braun, C. (1999). The polar average reference effect: A bias in estimating the head surface integral in EEG recording. Clinical Neurophysiology, 110(6), 1149–55.
Junghofer, M. , Elbert, T. , Tucker, D. M. , & Rockstroh, B. (2000). Statistical control of artifacts in dense array EEG/MEG studies. Psychophysiology, 37(4), 523–32.
Keil, A. , Bradley, M. M. , Hauk, O. , Rockstroh, B. , Elbert, T. , & Lang, P. J. (2002). Large-scale neural correlates of affective picture processing. Psychophysiology, 39(5), 641–49.
Keil, A. , Bradley, M. M. , Junghoefer, M. , Russmann, T. , Lowenthal, W. , & Lang, P. J. (2007). Cross-modal attention capture by affective stimuli: Evidence from event-related potentials. Cognitive, Affective, & Behavioral Neuroscience, 7(1), 18–24.
Keil, A. , Gruber, T. , Muller, M. M. , Moratti, S. , Stolarova, M. , Bradley, M. M. , et al. (2003). Early modulation of visual perception by emotional arousal: Evidence from steady-state visual evoked brain potentials. Cognitive, Affective, & Behavioral Neuroscience, 3(3), 195–206.
Keil, A. , Smith, J. C. , Wangelin, B. , Sabatinelli, D. , Bradley, M. M. , & Lang, P. J. (2008). Electrocortical and electrodermal responses co-vary as a function of emotional arousal: A single-trial analysis. Psychophysiology, 45(4), 511–15.
Keil, A. , Stolarova, M. , Heim, S. , Gruber, T. , & Muller, M. M. (2003). Temporal stability of high-frequency brain oscillations in the human EEG. Brain Topography, 16(2), 101–10.
Keil, A. , Stolarova, M. , Moratti, S. , & Ray, W. J. (2007). Adaptation in visual cortex as a mechanism for rapid discrimination of aversive stimuli. Neuroimage, 36, 472–79.
Klimesch, W. , Sauseng, P. , & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53(1), 63–88.
Knott, J. R. , & Irwin, D. A. (1968). Anxiety, stress and contingent negative variation (CNV). Electroencephalography and Clinical Neurophysiology, 24(3), 286–87.
Kolassa, I. , Kolassa, S. , Musial, F. , & Miltner, W. H. (2007). Event-related potentials to schematic faces in social phobia. Cognition and Emotion, 21(8), 1721–44.
Kolassa, I. T. , & Miltner, W. H. (2006). Psychophysiological correlates of face processing in social phobia. Brain Research, 1118(1), 130–41.
Kranczioch, C. , Debener, S. , Maye, A. , & Engel, A. K. (2007). Temporal dynamics of access to consciousness in the attentional blink. Neuroimage, 37(3), 947–55.
Lang, P. J. (1994). The motivational organization of emotion: Affect-reflex connections. In S. H. M. Van Goozen , N. E. Van de Poll , & J. E. Sergeant (Eds.), Emotions: Essays on emotion theory (pp. 61–93). Hillsdale, NJ: Erlbaum.
Lang, P. J. , Bradley, M. M. , & Cuthbert, B. N. (2005). International Affective Picture System: Technical manual and affective ratings. Gainesville, FL: NIMH Center for the Study of Emotion and Attention.
LeDoux, J. E. (1993). Emotional networks in the brain. In J. M. H. Lewis (Ed.), Handbook of emotions. (pp. 109–18). New York: Guilford Press.
Lesse, H. (1957). Amygdoloid electrical activity during a conditioned response. Paper presented at the International Congress of Electroencephalography and Clinical Neurophysiology, Brussels.
Linden, D. E. (2005). The p300: Where in the brain is it produced and what does it tell us? Neuroscientist, 11(6), 563–76.
Lindsley, D. B. (1950). Emotions and the electroencephalogram. In M. Reymert (Ed.), Feelings and emotions; The Mooseheart Symposium (pp. 238–46). New York: McGraw-Hill.
Luck, S. J. (2005). An introduction to the event-related potential technique. Cambridge, MA: MIT Press.
Luo, Q. , Mitchell, D. , Cheng, X. , Mondillo, K. , McCaffrey, D. , Holroyd, T. , et al. (2009). Visual awareness, emotion, and gamma band synchronization. Cerebral Cortex, 19(8), 1896–1904.
Müller, M. M. , Andersen, S. , & Keil, A. (2008). Time course of competition for visual processing resources between emotional pictures and a foreground task. Cerebral Cortex, 18, 1892–99.
Müller, M. M. , Teder-Salejarvi, W. , & Hillyard, S. A. (1998). The time course of cortical facilitation during cued shifts of spatial attention. Nature Neuroscience, 1(7), 631–34
Makeig, S. , Debener, S. , Onton, J. , & Delorme, A. (2004). Mining event-related brain dynamics. Trends in Cognitive Sciences, 8(5), 204–10.
Makeig, S. , Jung, T. P. , Bell, A. J. , Ghahremani, D. , & Sejnowski, T. J. (1997). Blind separation of auditory event-related brain responses into independent components. Proceedings of the National Academy of Sciences, 94, 10979–84.
Maris, E. (2012). Statistical testing in electrophysiological studies. Psychophysiology, 9(4), 549–65.
Melcher, J. R. , & Cohen, D. (1988). Dependence of the MEG on dipole orientation in the rabbit head. Electroencephalography and Clinical Neurophysiology, 70(5), 460–72.
Miller, J. , Patterson, T. , & Ulrich, R. (1998). Jackknife-based method for measuring LRP onset latency differences. Psychophysiology, 35(1), 99–115.
Moratti, S. , & Keil, A. (2005). Cortical activation during Pavlovian fear conditioning depends on heart rate response patterns: An MEG study. Brain Research: Cognitive Brain Research, 25(2), 459–71.
Moratti, S. , & Keil, A. (2009). Not what you expect: Experience but not expectancy predicts conditioned responses in human visual and supplementary cortex. Cerebral Cortex, 19(12), 2803–9.
Moratti, S. , Clementz, B. , Ortiz, T. , & Keil, A. (2007). Neural mechanisms of evoked oscillations: Stability and interaction with transient events. Human Brain Mapping, 28(12), 1318–33.
Moratti, S. , Keil, A. , & Miller, G. A. (2006). Fear but not awareness predicts enhanced sensory processing in fear conditioning. Psychophysiology, 43(2), 216–26.
Moratti, S. , Keil, A. , & Stolarova, M. (2004). Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks. Neuroimage, 21(3), 954–64.
Nitschke, J. B. , Miller, G. A. , & Cook, E. W. (1998). Digital filtering in EEG/ERP analysis: Some technical and empirical comparisons. Behavior Research Methods Instruments & Computers, 30(1), 54–67.
Nunez, P. L. , & Srinivasan, R. (2006). Electric fields of the brain (2nd ed.). New York: Oxford University Press.
Nunez, P. L. , Srinivasan, R. , Westdorp, A. F. , Wijesinghe, R. S. , Tucker, D. M. , Silberstein, R. B. , et al. (1997). EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. Electroencephalography and Clinical Neurophysiology, 103(5), 499–515.
Olejniczak, P. (2006). Neurophysiologic basis of EEG. Journal of Clinical Neurophysiology, 23(3), 186–89.
Pascual-Marqui, R. D. , Michel, C. M. , & Lehmann, D. (1994). Low resolution electromagnetic tomography: A new method for localizing electrical activity in the brain. International Journal of Psychophysiology, 18(1), 49–65.
Pascual-Marqui, R. D. , Michel, C. M. , & Lehmann, D. (1995). Segmentation of brain electrical activity into microstates: Model estimation and validation. IEEE Transactions of Biomedical Engineering, 42(7), 658–65.
Peyk, P. , Schupp, H. T. , Elbert, T. , & Junghofer, M. (2008). Emotion processing in the visual brain: A MEG analysis. Brain Topography, 20(4), 205–215.
Pizzagalli, D. , Lehmann, D. , Koenig, T. , Regard, M. , & Pascual-Marqui, R. D. (2000). Face-elicited ERPs and affective attitude: Brain electric microstate and tomography analyses. Clinical Neurophysiology, 111(3), 521–31.
Pizzagalli, D. A. , Greischar, L. L. , & Davidson, R. J. (2003). Spatio-temporal dynamics of brain mechanisms in aversive classical conditioning: High-density event-related potential and brain electrical tomography analyses. Neuropsychologia, 41(2), 184–94.
Pourtois, G. , Grandjean, D. , Sander, D. , & Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14(6), 619–33.
Radilova, J. (1982). The late positive component of visual evoked response sensitive to emotional factors. Act Nerv Super (Praha), 3(Suppl., Pt. 2), 334–37.
Ravden, D. , & Polich, J. (1999). On P300 measurement stability: Habituation, intra-trial block variation, and ultradian rhythms. Biological Psychology, 51(1), 59–76.
Regan, D. (1989). Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine. New York: Elsevier.
Sabatinelli, D. , Lang, P. J. , Keil, A. , & Bradley, M. M. (2007). Emotional perception: Correlation of functional MRI and event related potentials. Cerebral Cortex, 17, 1066–73.
Scherg, M. , & Von Cramon, D. (1986). Evoked dipole source potentials of the human auditory cortex. Electroencephalography and Clinical Neurophysiology, 65(5), 344–60.
Schupp, H. T. , Cuthbert, B. N. , Bradley, M. M. , Birbaumer, N. , & Lang, P. J. (1997). Probe P3 and blinks: Two measures of affective startle modulation. Psychophysiology, 34(1), 1–6.
Schupp, H. T. , Cuthbert, B. N. , Bradley, M. M. , Hillman, C. H. , Hamm, A. O. , & Lang, P. J. (2004). Brain processes in emotional perception: Motivated attention. Cognition and Emotion, 18(5), 593–611.
Schupp, H. T. , Junghofer, M. , Weike, A. I. , & Hamm, A. O. (2003). Emotional facilitation of sensory processing in the visual cortex. Psychological Science, 14(1), 7–13.
Simons, R. F. , & Miles, M. A. (1990). Nonfamilial strategies for the identification of subjects at risk for severe psychopathology: Issues of reliability in the assessment of event-related potentials (ERP). In J. W. Rohrbaugh , R. Parasuraman , & R. J. Johnson (Eds.), Event-related brain potentials: Basic issues and applications (pp. 343–63). Amsterdam: Elsevier.
Singer, W. , Engel, A. K. , Kreiter, A. K. , Munk, M. H. J. , Neuenschwander, S. , & Roelfsema, P. R. (1997) Neuronal assemblies: Necessity, signature and detectability. Trends in Cognitive Sciences, 1, 252–61.
Stolarova, M. , Keil, A. , & Moratti, S. (2006). Modulation of the C1 visual event-related component by conditioned stimuli: Evidence for sensory plasticity in early affective perception. Cerebral Cortex, 16(6), 876–87.
Tallon-Baudry, C. , & Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends in Cognitive Sciences, 3(4), 151–62.
Tenke, C. E. , & Kayser, J. (2005). Reference-free quantification of EEG spectra: Combining current source density (CSD) and frequency principal components analysis (fPCA). Clinical Neurophysiology, 116(12), 2826–46.
Tomarken, A. J. , Davidson, R. J. , Wheeler, R. E. , & Kinney, L. (1992). Psychometric properties of resting anterior EEG asymmetry: Temporal stability and internal consistency. Psychophysiology, 29(5), 576–92.
Walter, W. G. (1967). The analysis, synthesis and identification of evoked responses and contingent negative variation (CNV). Electroencephalography and Clinical Neurophysiology, 23(5), 489.
Weisz, N. , Kostadinov, B. , Dohrmann, K. , Hartmann, T. , & Schlee, W. (2007). Tracking short-term auditory cortical plasticity during classical conditioning using frequency-tagged stimuli. Cerebral Cortex, 17(8), 1867–76.
Wennberg, R. , Valiante, T. , & Cheyne, D. (2011). EEG and MEG in mesial temporal lobe epilepsy: Where do the spikes really come from? Clinical Neurophysiology, 122(7), 1295–1313.
Whittingstall, K. , & Logothetis, N. K. (2009). Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron, 64(2), 281–89.
Wieser, M. J. , McTeague, L. M. , & Keil, A. (2011). Sustained preferential processing of social threat cues: Bias without competition? Journal of Cognitive Neuroscience, 23(8), 1973–86.
Wieser, M. J. , Pauli, P. , Reicherts, P. , & Muhlberger, A. (2010). Don't look at me in anger! Enhanced processing of angry faces in anticipation of public speaking. Psychophysiology, 47(2), 271–80.
Yuval-Greenberg, S. , Tomer, O. , Keren, A. S. , Nelken, I. , & Deouell, L. Y. (2008). Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron, 58(3), 429–41.