ReviewTowards the utilization of EEG as a brain imaging tool
Highlights
► EEG is a cost-effective, easy-to-use brain imaging method. ► EEG spatial analyses render unambiguous neurophysiologic interpretability. ► EEG source imaging can be readily applied in clinical and experimental settings.
Introduction
Over 80 years ago the EEG was first described with the promise of it providing a “window into the brain” (Berger, 1929). However, the transparency of this window has been obscured in the sense that the sources in the brain that produced the signals on the scalp were not readily visible. Recent advances in EEG recording technology and EEG analysis methods made this window much more transparent, and the signal–source relationship has become clearer. In this review we overview some of the basic methods that render EEG a comprehensive and powerful brain-imaging tool that directly maps the brain neuronal activity with reasonable spatial and superb temporal resolution.
During the largest part of the 80 years of existence of EEG, and unfortunately to some extent still today, the analytic potential of EEG has not been fully exploited. On the contrary, several serious misunderstandings about the generation of the scalp potentials have led to wrong interpretations of the data and to claims about brain functions that were later falsified by intracranial recordings, lesion studies, or neuroimaging methods; thereby severely discrediting EEG.
Such misinterpretations were mainly due to the ignorance of important physical principles that underlie the measurement of electric potentials at the scalp surface. Most important is the fact that a given electrode on the scalp does not record solely the neuronal activity directly underlying it. Rather, every electrode picks up signals from different sources that can eventually be quite distal. This is because the electric field of each active source in the brain spreads in all directions and is thus picked up to a variable extent by each electrode. This also holds for the reference electrode against which the potential at one scalp electrode is compared. Fluctuation of the voltage at the reference electrode will lead to changes of the potential at the active electrode even if the voltage at that point was actually stable. There is no point that is electrically silent and could be considered as true zero potential. Thus, changing the reference position will change the absolute potential at the active electrode because EEG forcibly entails recording potential differences. This reference-dependent feature of EEG potentials is often cited as a major drawback of EEG as compared for example to MEG (Hari, 2011).
However, it is important to note and to insist on the fact that the topography of the potential field is completely independent of the choice of the reference (Geselowitz, 1998). Because it is the topography of the electric or magnetic field that is the only relevant information used for electric or magnetic source imaging, the so-called “reference-problem” of the EEG effectively does not exist and a search for an optimal reference (Gencer et al., 1996) for source imaging is meaningless.
In this article we overview EEG analysis methods that are based on the understanding of the biophysical principles that lead to the potential field on the scalp and that are quantifying the properties of this potential field in time and in space. Analysis methods that are based on single channel waveforms are not considered here, because such analyses are ambiguous with respect to 1) the underlying generators as well as more general neurophysiologic causes and 2) the statistical confidence that can be placed on them (Michel et al., 2009, Murray et al., 2008, Murray et al., 2009).
Section snippets
Principles of EEG spatial analysis
The EEG is traditionally analyzed in terms of temporal waveforms at certain channels, looking at power of rhythms in the spontaneous EEG, at amplitude and latency of the peaks and troughs in event-related potentials (ERPs), or at particular grapho-elements in pathological or sleep stages. There is no doubt that this type of analysis has provided many important insights regarding brain functioning in health and disease, but it has not been considered as an imaging method in the sense that one
Spatial analysis of the EEG at rest
In recent years the term “Resting State” has been established and has received considerable attention in the brain imaging literature (Fox and Raichle, 2007). It mainly refers to the coherent fluctuations of blood oxygen level dependent (BOLD) responses in different brain regions measured with fMRI, while the subject is at rest without any particular stimulus or task. Using independent component analysis, distinct patterns of coherent activity in large-scale networks have been identified,
Spatial analysis of multichannel stimulus-related activity
Aside from the analysis of spontaneous EEG, there is also a considerable body of research that focuses on stimulus-related brain activity with a particular interest in how and when the brain processes specific types of information and/or generates decisions or actions in response to external stimuli in conjunction with mental operations. This line of enquiry into mental chronometry stems in large part from the pioneering efforts of Donders and later Sternberg (reviewed in Vaughan, 1990). Their
Clinical applications of spatial EEG analysis
The spatial analysis methods of multichannel EEG described in this review have been applied to a wide range of clinical populations, and we review only a selected sampling here.
Conclusions and outlook
The aim of this review was to illustrate the paradigm change that took place with respect to the EEG analysis in the last decade or so. EEG analysis moved away from the traditional analysis of grapho-elements at certain electrodes to a comprehensive analysis of the brain's electric field at the scalp. This movement was certainly largely inspired by MEG work, which from the onset rather analyzed the spatial than the temporal patterns. We tried to show here that spatial EEG analysis is not solely
Acknowledgments
The authors receive support from the Swiss National Science Foundation (grants 310030-132952 and 33CM30-124089 to CMM, grants 310030B-133136, K-33K1_122518, and 320030_120579 to MMM as well as the NCCR SYNAPSY grant to CMM and MMM).
References (183)
- et al.
Evidence for dissociation of spatial and nonspatial auditory information processing
Neuroimage
(2001) The conscious access hypothesis: origins and recent evidence
Trends Cogn. Sci.
(2002)Large-scale cortical networks and cognition
Brain Res. Brain Res. Rev.
(1995)- et al.
Operational principles of neurocognitive networks
Int. J. Psychophysiol.
(2006) - et al.
BOLD correlates of EEG topography reveal rapid resting-state network dynamics
Neuroimage
(2010) - et al.
Accuracy of EEG source imaging of epileptic spikes in patients with large brain lesions
Clin. Neurophysiol.
(2009) - et al.
Are the electroencephalograms mainly rhythmic? Assessment of periodicity in wide-band time series
Neuroscience
(2003) - et al.
Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework
Cognition
(2001) The minimum duration of a perception
Neuropsychologia
(1970)- et al.
Common reference coherence data are confounded by power and phase effects
Electroencephalogr. Clin. Neurophysiol.
(1988)
The functional anatomy of the MMN: a DCM study of the roving paradigm
Neuroimage
Optimal reference electrode selection for electric source imaging
Electroencephalogr. Clin. Neurophysiol.
Combination of EEG-fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistent focal epilepsies
Neuroimage
The temporal structures and functional significance of scale-free brain activity
Neuron
Spatial versus object feature processing in human auditory cortex: a magnetoencephalographic study
Neurosci. Lett.
Native EEG and treatment effects in neuroleptic-naive schizophrenic patients: time and frequency domain approaches
Schizophr. Res.
Resting-state EEG in schizophrenia: auditory verbal hallucinations are related to shortening of specific microstates
Clin. Neurophysiol.
Impaired early visual response modulations to spatial information in chronic schizophrenia
Psychiatry Res.
Decreased functional connectivity of EEG theta-frequency activity in first-episode, neuroleptic-naive patients with schizophrenia: preliminary results
Schizophr. Res.
Topographic time-frequency decomposition of the EEG
Neuroimage
Millisecond by millisecond, year by year: normative EEG microstates and developmental stages
Neuroimage
Decreased EEG synchronization in Alzheimer's disease and mild cognitive impairment
Neurobiol. Aging
Spatio-temporal dynamics of olfactory processing in the human brain: an event-related source imaging study
Neuroscience
Multichannel topography of human alpha EEG fields
Electroencephalogr. Clin. Neurophysiol.
Intracerebral dipole source localization for FFT power maps
Electroencephalogr. Clin. Neurophysiol.
Reference-free identification of components of checkerboard-evoked multichannel potential fields
Electroencephalogr. Clin. Neurophysiol.
Averaging of spectral power and phase via vector diagram best fits without reference electrode or reference channel
Electroencephalogr. Clin. Neurophysiol.
EEG alpha map series: brain micro-states by space-oriented adaptive segmentation
Electroencephalogr. Clin. Neurophysiol.
Sensitivity of MEG and EEG to source orientation
Brain Topogr.
Task-modulated “what” and “where” pathways in human auditory cortex
Proc. Natl. Acad. Sci. U.S.A.
“What” and “where” in the human auditory system
Proc. Natl. Acad. Sci. U.S.A.
Estimation of the cortical connectivity by high-resolution EEG and structural equation modeling: simulations and application to finger tapping data
IEEE Trans. Biomed. Eng.
Comparison of different cortical connectivity estimators for high-resolution EEG recordings
Hum. Brain Mapp.
Neuroelectrical hyperscanning measures simultaneous brain activity in humans
Brain Topogr.
Atoms of thought
Print-specific multimodal brain activation in kindergarten improves prediction of reading skills in second grade
Neuroimage
Electromagnetic brain mapping
IEEE Signal Process. Mag.
Abnormal cortical network activation in human amnesia: a high-resolution evoked potential study
Brain Topogr.
Über das Elektroenkephalogramm des Menschen
Arch. Psychiatr. Nervenkr.
Noise in brain activity engenders perception and influences discrimination sensitivity
Journal of Neuroscience
Which Physiological Components are More Suitable for Visual ERP Based Brain-Computer Interface? A Preliminary MEG/EEG Study
Brain Topogr
Toward discovery science of human brain function
Proc. Natl. Acad. Sci. U.S.A.
Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function?
Ann. N. Y. Acad. Sci.
Preserved feedforward but impaired top-down processes in the vegetative state
Science
Scopolamine effects on visual information processing, attention, and event-related potential map latencies
Psychophysiology
Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients
Brain
Electrical source imaging for presurgical focus localization in epilepsy patients with normal MRI
Epilepsia
Spatiotemporal analysis of multichannel EEG: CARTOOL
Comput. Intell. Neurosci.
Rhythms of the Brain
Cited by (506)
Electroencephalography findings in menstrually-related mood disorders: A critical review
2024, Frontiers in NeuroendocrinologyOn a Calderón preconditioner for the symmetric formulation of the electroencephalography forward problem without barycentric refinements
2023, Journal of Computational PhysicsEffects of noise and noise reduction on audiovisual speech perception in cochlear implant users: An ERP study
2023, Clinical Neurophysiology