Magnetoencephalography in Pediatric Neuroimaging
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Developmental Science 5:3 (2002), pp 361–370 MagnetoencephalographyBlackwell Publishers Ltd in pediatric neuroimaging Ritva Paetau Department of Child Neurology, Hospital for Children and Adolescents, University of Helsinki; Brain Research Unit, Helsinki University of Technology; BioMag Laboratory; Helsinki University Central Hospital, Finland Abstract Neural currents give rise to electroencephalogram (EEG) and magnetoencephalogram (MEG). MEG has selective sensitivity to tangential currents (from fissural cortex), and less distorted signals compared with EEG. A major goal of MEG is to determine the location and timing of cortical generators for event-related responses, spontaneous brain oscillations or epileptiform activity. MEG provides a spatial accuracy of a few mm under optimal conditions, combined with an excellent submillisecond temporal resolution, which together enable spatiotemporal tracking of distributed neural activities, e.g. during cognitive tasks or epileptic discharges. While the present focus of pediatric MEG is on tailored epilepsy surgery, the complete noninvasiveness of MEG also provides unlimited possibilities to study the brain functions of healthy and developmentally deviant children. Introduction 1996; Kamada, Moller, Saguer, Kassubek, Kaltenhauser, Kober, Uberall, Lauffer, Wenzel & Vieth, 1998; Kubota, Magnetoencephalography (MEG) detects weak extra- Takeshita, Sakakihara & Yangisawa, 2000), on the Landau- cranial magnetic fields, and allows determination of Kleffner syndrome and related disorders (Paetau, Kajola, their intracranial sources. Magnetic source imaging Korkman, Hämäläinen, Granström & Hari, 1991; Paetau, (MSI) means procedures which combine the MEG 1994; Lewine, Andrews, Chez, Patil, Devinsky, Smith, Kan- sources with anatomical magnetic resonance imaging ner, Davis, Funke, Jones, Chong, Provencal, Weisend, Lee & (MRI). The term MEG is used in the present paper to Orrison, 1999; Paetau, Granström, Blomstedt, Jousmäki, cover both MEG and MSI. Korkman & Liukkonen, 1999; Sobel, Aung, Otsubo & After the first recordings of human magnetic alpha Smith, 2000), on sensory cortex properties in progressive rhythm (Cohen, 1968), MEG technology and its appli- myoclonus epilepsies (Karhu, Hari, Paetau, Kajola & cations to neuroscience and clinical research have pro- Mervaala, 1994; Lauronen, 2001; Forss, Silen & Kar- gressed at an accelerating rate during the past 20 years. jalainen, 2001), and on dyslexia (Heim, Eulitz, Several excellent reviews are available on various aspects Kaufmann, Fuchter, Pantev, Lamprecht-Dinnesen, Matulat, of the MEG method (e.g. Williamson & Kaufman, 1981; Scheer, Borstel & Elbert, 2000; Simos, Breier, Fletcher, Weinberg, Stroink & Katila, 1985; Hari & Ilmoniemi, Bergman & Papanicolaou, 2000). This article will briefly 1986; Sato, Balish & Muratore, 1991; Hämäläinen, Hari, review the basic principles of MEG and give some exam- Ilmoniemi, Knuutila & Lounasmaa, 1993; Gallen, Hir- ples of the present use of MEG in children. schkoff & Buchanan, 1995; Lewine & Orrison Jr., 1995; Hari, 1998; Forss, Nakasato, Ebersole, Nagamine & Salmelin, 2000; Otsubo & Snead, 2001). At present, over Basic principles of MEG one hundred MEG installations worldwide contribute to our knowledge about the function and development A moving electric charge is always associated with an of the human brain. Most MEG studies have been electric field and a concomitant magnetic field surround- conducted with adult subjects, but some MEG data ing the axis of movement (Figure 1a). Electroencephalo- already exist on children. Pediatric MEG studies have gram (EEG) and MEG signals are believed to reflect mainly focused on epilepsy surgery (Paetau, Hämäläinen, synchronous postsynaptic currents in thousands of par- Hari, Kajola, Karhu, Larsen, Lindahl & Salonen, 1994; allel apical dendrites. Despite being ultimately due to the Chuang, Otsubo, Hwang, Orrison & Lewine, 1995; same primary currents, EEG and MEG signals differ at Minassian, Otsubo, Weiss, Elliott, Rutka & Snead, 1999), some important points. First, only tangential currents, on rolandic epilepsy (Kubota, Oka, Kin & Sakakihara, parallel to the head surface, give rise to an extracranial 1996; Minami, Gondo, Yamamoto, Yanai, Tasaki & Ueda, magnetic field. Because the apical dendrites typically run Address for correspondence: Hospital for Children and Adolescents, P.O. Box 280, FIN-00029 HUS, Finland; e-mail: ritva.paetau@hus.fi © Blackwell Publishers Ltd. 2002, 108 Cowley Road, Oxford OX4 1JF, UK and 350 Main Street, Malden, MA 02148, USA. 362 Ritva Paetau Therefore, tumors, cysts, calcified lesions and skull defects cause less distortion on MEG than EEG signals (van der Broek, Reinders, Donderwinkel & Peters, 1998). Third, signal attenuation in EEG is caused by poorly conducting tissue, while the magnetic field fades off proportionally to the second power of the distance from the source. Infants and persons with small heads should preferably be studied with systems composed of two part-head devices adjustable according to the head size or with specially designed baby devices. Fourth, different practical problems hamper data acquisition. MEG sen- sors are in a rigid helmet and the head has to be kept immobile with respect to the helmet. Long-term record- ings or recordings of major motor seizures are so far not possible with MEG, but continuous monitoring of the head position may offer relief to some of the movement problems. Finally, MEG and EEG have partly differing artifact profiles: MEG is less sensitive to muscle artifacts than EEG. On the other hand, magnetic materials mov- ing with respiration (traces from craniotomy drills, some shunt materials, tooth braces, cochlear implants, etc.) may cause serious artifacts or even destroy the MEG data. Instrumentation The brain’s magnetic fields are extremely weak (on the − Figure 1 Physical basis of MEG signals. (a) The intracellular order of 10 15 Tesla) and need to be heavily amplified, current I in the apical dendrite of a pyramidal cell is associated while much stronger environmental magnetic noise from with a surrounding magnetic field B. (b) In the brain, pyramidal power lines or electronic equipment must be suppressed. cells typically are perpendicular to cortex surface, and may be MEG measurements are carried out in magnetically radial (white arrows), oblique or tangential (dark arrows) to the shielded rooms, using sensitive superconducting quan- scalp. Only the tangential currents and the tangential tum interference devices (SQUIDs) (Zimmermann, Thiene component of oblique currents contribute to the extracranial & Harding, 1970). The MEG sensors consist of a flux magnetic field, which can be detected by sensitive SQUID transformer coupled to a SQUID, which amplifies the magnetometers. (c) Dipolar magnetic field pattern viewed from above. B in indicates the magnetic flux into the head and B weak extracranial magnetic field and transforms it into out the flux out from the head. An equivalent current dipole voltage. The sensors are immersed in liquid helium and (ECD; the thick black arrow) represents the concerted action attached on a concave bottom of a container, where they of all fissural dipoles. Its orientation is parallel to the isofield typically lie at a distance of 3–4 cm from the cortex. lines and it is located underneath the steepest gradient halfway A flux transformer may be planar, and gives the between the in- and out-flowing flux. Its depth determines the largest signal at the sharpest field gradient right above distance between the two extremes, and its strength is a local brain current, or axial giving maximum signals proportional to the number of active pyramidal cells. at both the field extremes. At present, several companies manufacture whole-head devices with 64–306 sensors for perpendicular to the cortex surface, MEG signals mainly clinical and experimental work. The present examples arise in fissure walls (Figure 1b). The EEG signals, on come from experiments with a planar 122-SQUID gradi- the other hand, are dominated by radial currents, while ometer, Neuromag-122™, and a planar-axial 306-SQUID the tangential ones may require signal averaging to be device Vectorview, 4-D Neuroimaging, Helsinki, Finland. detected. This complementary sensitivity to current orientation warrants combined use of EEG and MEG Data acquisition whenever possible. Second, inhomogeneous tissue con- ductivity of the human head tends to spread out the During the experiments, the subject is sitting or lying EEG signal, but does not alter the magnetic fields. with his/her head inside a sensor helmet as close to the © Blackwell Publishers Ltd. 2002 Magnetoencephalography 363 sensors as possible. Head movements are minimized by Brain–muscle interaction can be studied using MEG- using videotape films, visual stimuli, neck collars or head EMG coherence analysis, an important new method for fixating bite bars. identification of the motor cortex (Salenius, Portin, The exact head position within the helmet is often Kajola, Salmelin & Hari, 1997; Mäkelä, Kirveskari, determined with three or four coils pasted around the Seppä, Hämäläinen, Forss, Avikainen, Salonen, Salenius, head. Prior to data acquisition, the position of these Kovala, Randell, Jääskeläinen & Hari, 2001). It requires coils is sensed with a 3-D digitizer within an individual a few minutes of weak voluntary isometric muscle head coordinate system based on three fiducial points: contraction, and can be successfully recorded from the left and right preauricular points and the