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Annotation: What Electrical Brain Activity Tells Us About Brain Function That Other Techniques Cannot Tell Us – a Child Psychiatric Perspective

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Annotation: What Electrical Brain Activity Tells Us About Brain Function That Other Techniques Cannot Tell Us – a Child Psychiatric Perspective Journal of Child Psychology and Psychiatry 48:5 (2007), pp 415–435 doi:10.1111/j.1469-7610.2006.01681.x Annotation: What electrical brain activity tells us about brain function that other techniques cannot tell us – a child psychiatric perspective Tobias Banaschewski1 and Daniel Brandeis2 1Child and Adolescent Psychiatry, University of Go¨ttingen, Germany; 2Child and Adolescent Psychiatry, and Centre for Integrative Human Physiology, University of Zu¨rich, Switzerland Background: Monitoring brain processes in real time requires genuine subsecond resolution to follow the typical timing and frequency of neural events. Non-invasive recordings of electric (EEG/ERP) and magnetic (MEG) fields provide this time resolution. They directly measure neural activations associated with a wide variety of brain states and processes, even during sleep or in infants. Mapping and source estimation can localise these time-varying activation patterns inside the brain. Methods: Recent EEG/ ERP research on brain functions in the domains of attention and executive functioning, perception, memory, language, emotion and motor processing in ADHD, autism, childhood-onset schizophrenia, Tourette syndrome, specific language disorder and developmental dyslexia, anxiety, obsessive- compulsive disorder, and depression is reviewed. Results: Over the past two decades, electrophysiology has substantially contributed to the understanding of brain functions during normal development, and psychiatric conditions of children and adolescents. Its time resolution has been important to measure covert processes, and to distinguish cause and effect. Conclusions: In the future, EEG/ERP para- meters will increasingly characterise the interplay of neural states and information processing. They are particularly promising tools for multilevel investigations of etiological pathways and potential predictors of clinical treatment response. Keywords: ADHD, anorexia nervosa, anxiety, autism, childhood-onset schizophrenia, depression, developmental dyslexia, EEG, endophenotypes, ERP, fMRI, neuropsycho- logy, obsessive-compulsive disorder, specific language disorder, tic disorder. Abbreviations: ACC: anterior cingulate gyrus; ADHD: attention deficit hyperactivity disorder; ASD: autism spectrum disorder; BOLD: blood-oxygen-level-dependent; CNV: contingent negative variation; COMT: Catechol- O-methyltransferase; CPT A-X: (cued) continuous performance test A-X (type); CHRM2: cholinergic receptor, muscarinic 2; DRD2: D2 receptor gene; EEG: electroencephalogram; ERN: error-related nega- tivity; ERP: event-related potential; fMRI: functional Magnetic Resonance Imaging; GABRA2: GABA-A receptor gene; LDAEP: loudness-dependent amplitude change of auditory evoked ERP; MDD: major depressive disorder; MEG: magnetoencephalogram; MMN: mismatch negativity; NIRS: Near Infrared Spectroscopy; PET: Positron Emission Tomography; REM: rapid eye movement; RP: readiness potential (or Bereitschaftspotential); SSRI: selective serotonine reuptake inhibitor. Electrophysiological and magnetencephalographic tributed substantially to our understanding of brain methods allow non-invasive monitoring of brain states and functions in normal development, and of processes in real time. Their supreme time resolu- deviations in psychiatric conditions occurring in tion captures even fast neural events and high- childhood or adolescence. frequency oscillations, and permits functional brain The paper starts with an introduction to meth- imaging at millisecond resolution through source odological issues and contrasts advantages and analysis of high density maps. As a consequence, disadvantages of electroencephalogram (EEG) and they can directly measure the full spatio-temporal event-related potentials (ERP) methodology with dynamics of neural activation (see: methodological those of other neuroimaging techniques and neuro- section) associated with a wide variety of cognitive psychology. Secondly, recent advances of EEG/ERP processes and their development, and can be used research in the domains of attention, executive repeatedly without problems in longitudinal studies functions, perception, memory, language, emotion, and even during sleep or in infants (for reviews see: and motor processing are reviewed. This selective Picton et al., 2000; Picton & Hillyard, 1988; Taylor & review is not comprehensive, but rather aims to Baldeweg, 2002). Over the past two decades, illustrate the key issues through exemplary findings electrophysiology has increasingly been used for in child psychiatry, focusing on ERP research. The investigating the biological substrates of psychiatric selection of studies was based (a) on the presence of disorders. findings that contribute to theoretical controversies The aim of this paper is to illustrate the current or clinical treatment issues, (b) on the quality of the state of the art of electrophysiological brain imaging samples investigated and the analyses used, and (c) (here: EEG and ERP) in child and adolescent psy- on whether a paper clearly illustrates specific chiatry. It will be shown how this research has con- methodological strengths or weaknesses of EEG/ Ó 2006 The Authors Journal compilation Ó 2006 Association for Child and Adolescent Mental Health. Published by Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA 416 Tobias Banaschewski and Daniel Brandeis ERP research. We only included those studies with depends on local cortical folding, and the underlying adults which were exemplary and lacked an analo- distributed neural networks which may involve a gous equivalent in child psychiatric findings. distributed pattern of activations and deactivations. In an outlook, the annotation will then give EEG waveforms generally are classified according examples how electrophysiological parameters have to their dominant frequency (see Table 1), ampli- been (or may be) used to predict pharmacological tude, shape, and the sites of scalp distribution treatment response and to identify endophenotypes (topography). for multilevel investigations of etiological pathways. The EEG frequency composition is highly heritable (van Beijsterveldt & van Baal, 2002). It reflects the state of development and wakefulness, along with Methodology modulations due to state regulation and arousal. The magnetoencephalogram (MEG) measures the The EEG measures brain electrical activity as corresponding magnetic fields with sensors around recorded from electrodes placed on the scalp. It di- the head. Although electric and magnetic fields are rectly reflects neural mass action, and mainly syn- typically closely related, the MEG is insensitive to chronised postsynaptic potentials of aligned neurons radial brain sources and skull conductivities, and such as pyramidal cells in cortex. Such spatio- less sensitive to deep sources, thus (compared to temporal synchronisation of neural networks results EEG recording) providing a more selective view of the in net polarisation of extended brain regions, which same neural mass activity. may be transient, slow, or oscillatory. The largest ERP are changes in the ongoing EEG or MEG EEG potentials are generated by cortical sources which are time-locked (i.e., stimulus- or response- which vary in depth and orientation, reflecting the locked) and phase-locked (i.e., time-locked and with cortical folding. The attenuation of EEG activity with the same polarities) to perceptual, cognitive, and depth is moderate, and far less than for the MEG. motor processes. They are typically extracted from The clinical routine of auditory brain stem potential the ongoing electroencephalogram by means of sig- recordings demonstrates that even activity from nal averaging (see glossary). Averaging not only small and deep subcortical structures is reliably eliminates the spontaneous background EEG, but detected in the scalp EEG after averaging (see below). also those event-related EEG modulations which are In contrast, action potentials are unlikely to con- not phase-locked as ‘noise’. Other techniques can tribute to the scalp EEG, because their fields are also characterise such event-related modulations of radially symmetric around the axons and thus can- specific frequencies (event-related synchronisation cel at some distance despite their large amplitude. or desynchronisation), stimulus-induced phase- Although an influential model has related surface locking (i.e., stability of the evoked EEG rhythms polarity of slow ERPs to neural inhibition (positivity, independently of amplitude measures), or the power as during the frontocentral NoGo P300) or activation (i.e., the ‘strength’) within defined frequency bands of (negativity, as during the pre-central CNV) of nearby the spontaneous EEG. cortical regions (Birbaumer, Elbert, & Canavan, ERP consist of characteristic sequences of com- 1990), tomographic source models of brain electrical ponents or ‘microstates’ (i.e., time segments with a activity (Pascual-Marqui, Michel, & Lehmann, 1994; stable topographical distribution of brain electrical Strik, Fallgatter, Brandeis, & Pascual-Marqui, 1998) activity) that span a continuum between early and fMRI correlates of slow ERPs (Hinterberger et al., activity primarily determined by the physical char- 2003) indicate a more complex relationship between acteristics of the eliciting stimulus (latency range the local polarity of scalp maps, which strongly <250 ms), and later components (latency range Table 1 Overview of EEG frequency bands, their topography, developmental and functional
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