Clinical Neurophysiology 123 (2012) 1581–1585
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph
Reconstruction of quasi-radial dipolar activity using three-component magnetic
field measurements
J. Haueisen a,b,c,⇑, K. Fleissig b, D. Strohmeier a, T. Elsarnagawy c, R. Huonker b, M. Liehr b, O.W. Witte b
a
Institute of Biomedical Engineering and Informatics, Faculty of Computer Science and Automation, Ilmenau University of Technology, Germany
Biomagnetic Center, Department of Neurology, University Hospital Jena, Erlanger Allee 101, 07747 Jena, Germany
c
Department of Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia
b
See Editorial, pages 1477–1478
a r t i c l e
i n f o
Article history:
Available online 8 February 2012
Keywords:
Magnetoencephalography
MEG
Primary somatosensory cortex
Median nerve
Three-component magnetic field
measurements
Vector magnetometer
h i g h l i g h t s
Novel vector-biomagnetometers enable reconstruction of quasi-radial brain activity.
We demonstrate this reconstruction of radial brain activity for Brodmann area 1 in the somatosensory
system.
Vector-biomagnetometers provide greater insight into brain activity than does standard
magnetoencephalography.
a b s t r a c t
Objective: While standard magnetoencephalographic systems record only one component of the biomagnetic field, novel vector-biomagnetometers enable measurement of all three components of the field at
each sensing point. Because information content in standard one-component magnetoencephalography
(MEG) is often not adequate to reconstruct quasi-radial dipolar activity, we tested the hypothesis that
quasi-radial activity can be estimated using three-component MEG.
Methods: We stimulated the right median nerve in 11 healthy volunteers and recorded the somatosensory evoked fields over the contralateral hemisphere using a novel vector-biomagnetometer system comprised of SQUID-based magnetometer triplets. Source reconstruction for the early cortical components
N20m and P25m was subsequently performed.
Results: Both tangential and quasi-radial dipolar activity could be reconstructed in 10 of the 11 participants. Dipole locations were found in the vicinity of the central sulcus, and dipole orientations were predominantly tangential for N20m and quasi-radial for P25m. The mean location difference between the
tangential and quasi-radial dipoles was 11.9 mm and the mean orientation difference was 97.5°.
Conclusions: Quasi-radial dipolar activity can be reconstructed from three-component magnetoencephalographic measurements.
Significance: Three-component MEG provides higher information content than does standard MEG.
Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights
reserved.
1. Introduction
Electroencephalography (EEG) and magnetoencephalography
(MEG) are non-invasive modalities for recording brain activity at
high temporal resolutions. Source reconstruction based on EEG
and MEG is a widely used technique in the neurosciences that al⇑ Corresponding author at: Ilmenau University of Technology, Institute for
Biomedical Engineering and Informatics, P.O. Box 100565, D-98684 Ilmenau,
Germany. Tel.: +49 3677 69 2861; fax: +49 3677 69 1311.
E-mail address: jens.haueisen@tu-ilmenau.de (J. Haueisen).
lows for spatio-temporal disentanglement of overlapping brain
activity. Dipolar source models are commonly employed to describe the electrical activity in a certain brain area. Although EEG
and MEG signals are generated by the same underlying bioelectric
sources, they have different sensitivities with respect to superficial
and deep sources, and also with respect to radial and tangential
sources (Goldenholz et al., 2009). Therefore, the two modalities
are used in combination to distinguish these sources (Jaros et al.,
2008; Wood et al., 1985).
Distinction between radially and tangentially oriented sources
is based on the local inner skull curvature; however, it has its cor-
1388-2457/$36.00 Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.clinph.2011.12.020
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J. Haueisen et al. / Clinical Neurophysiology 123 (2012) 1581–1585
respondence in the cortical anatomy, too. Tangential brain activity
originates mainly from the walls of the sulci, while radial brain
activity originates mainly from the crown of the gyri or the bottom
of the sulci.
Baule and McFee (1965) showed that a radial electric dipole in a
spherical volume conductor does not produce a magnetic field
outside the sphere. However, in a realistic volume conductor,
radial dipoles also produce magnetic fields outside the volume
conductor (Cohen and Cuffin, 1991; Cohen et al., 1990; Melcher
and Cohen, 1988). In additional, strictly radial dipoles would occur
in only a few real cases, as the dipoles are commonly slightly tilted
relative to the radial direction because of the anatomical structure
of the cortex and the extent of most activities (Murakami and Okada, 2006), or because of non-spherical local skull curvature.
Throughout this study, we use the term quasi-radial dipole to
describe the radial dipole in a realistic volume conductor.
One specific property of MEG is its lower sensitivity to quasi-radial sources than tangential sources (Cohen and Cuffin, 1983). It has
been shown both experimentally (Melcher and Cohen, 1988) and in
simulation studies (Haueisen et al., 1995) that quasi-radially
oriented dipoles produce magnetic fields that are 4–10 times weaker outside the head than those from tangentially oriented dipoles in
the same position; thus, MEG is considered inappropriate for localization of quasi-radial sources due to low SNR. However, only one
component of the vectorial biomagnetic field has been used in previous studies. Whole head biomagnetometer typically measure the
component of the magnetic field approximately normal to the head
surface (Br). Flat bottom biomagnetometer typically measure the
component of the magnetic field normal to the bottom of the cryostat (Bz). Recently developed vector-biomagnetometers (Burghoff
et al., 1999; Kobayashi and Uchikawa, 2001; Liehr and Haueisen,
2008; Schnabel et al., 2004) enable recording of all three vectorial
components of the biomagnetic field. Measurements (Kobayashi
and Uchikawa, 2001) and simulations (Arturi et al., 2004) showed
a higher information content for data from vector-biomagnetometers than for those with standard biomagnetometers.
The aim of this study is to investigate experimentally the feasibility of reconstructing quasi-radially oriented dipoles based on
vectorial measurements of biomagnetic fields. We chose the
somatosensory system for investigation because of its well-known
generator structure of tangential (Brodmann area 3b) and quasi-radial (Brodmann area 1) dipolar sources that overlap in time.
2. Methods
2.1. Participants and measurements
Eleven healthy volunteers (6 males, 5 females; age, 27.4 ±
5.2 years), 10 right-handed and one left-handed, underwent examination with the ARGOS 200 vector-biomagnetometer (AtB SrL, Pescara, Italy) positioned over the somatosensory cortex. The median
nerve was stimulated contralateral to the magnetic recording site
[stimulation strength: motor threshold plus sensor threshold
(Mauguière et al., 1999); constant current square wave impulses
with a length of 200 ls]. Stimulus onset asynchrony was randomized between 0.7 and 1.4 s. A total of 512 epochs was averaged.
Data were sampled at 1025 Hz with a hardware low-pass filter of
256.25 Hz. ECG, and horizontal and vertical EOG were recorded to
detect artifacts.
Isotropic T1-weighted magnetic resonance (MR) images of the
brain with resolution of 1 mm were obtained from each participant
to provide realistic head modeling for the source localization procedure. Co-registration between MR and MEG coordinate systems
was obtained by digitizing and rigidly transforming anatomical
landmarks (nasion, left and right pre-auricular points).
Fig. 1. ARGOS 200 sensor configuration. The triplets are distributed over four levels.
The lowest level (which is the main measurement plane) is a planar sensor array
consisting of 56 sensor triplets laid out on a hexagonal grid, covering a circular
planar surface with a diameter of approximately 25 cm. The second level contains
seven triplets, and the third and fourth levels contain one triplet each. The second
level is on a plane oriented parallel to the measurement plane at a distance of
98 mm. The third level is 196 mm above the first plane, and the fourth level is
254 mm above the first plane. The center (cube corner point) of the triplets in the
third and fourth levels is located at the x, y position (0, 0). The triplets located in the
second, third, and fourth levels are used for noise cancelation.
The study was approved by the Ethics Committee of the medical
faculty of the Friedrich Schiller University Jena. All participants
gave their written informed consent.
2.2. Vector-biomagnetometer
The vector-biomagnetometer used included 195 superconducting quantum interference devices (SQUIDs). Sensors were fully
integrated planar SQUID magnetometers produced using Nb technology with integrated pick-up loops. The sensing area for each of
the 195 sensors was a square of 8 mm side length. The intrinsic
noise level of the SQUIDs was below 5 fT Hz 1/2 at 10 Hz.
Triaxial vector magnetometers were formed by grouping three
basic sensor elements into a triplet. The three square sensor elements in each triplet were arranged perpendicular to each other
on the three adjacent planes of one corner of a cube (Fig. 1 inset),
enabling measurement of the magnetic field vector. There are two
identical but rotated versions of the triplets, in order to realize a
dense arrangement of the triplets (Fig. 1). Thus, six components
of the magnetic field were measured [Ba1, Bb1, Bc1] and [Ba2, Bb2, Bc2],
where the indices 1 and 2 indicate the two rotated triplets (Moraru
et al., 2011). To ensure that all three SQUIDs were located a similar
distance from the bottom of the measurement system, this corner
of the cube was placed closest to the bottom of the cryostat (with
the cube standing on this corner). An additional advantage of this
arrangement is that the commonly measured Bz component (i.e.
perpendicular to the cryostat bottom) of the magnetic field can be
obtained simply by adding the magnetic flux vectors measured by
the three SQUIDs and projecting the sum vector onto the common
device axis. Fig. 1 shows the schematics of the sensor setup.
The SQUID electronics have a dynamic range of 22 bits, with a
lowest resolution of 2.05 fT and range of ±4.31 nT. The system
was installed in a magnetically shielded room with three layers
of highly permeable material and one layer of aluminum (AtB
SrL, Pescara, Italy). The shielding performance was 38 dB at 1 Hz
and 80 dB at 20 Hz.
J. Haueisen et al. / Clinical Neurophysiology 123 (2012) 1581–1585
For visualization purposes and to allow for better comparison
with the literature, local [Ba1, Bb1, Bc1] and [Ba2, Bb2, Bc2] at each
triplet were transformed to global [Bx, By, Bz] values for each triplet.
2.3. Source localization
A realistic one-compartment boundary element model was
derived for each volunteer, to serve as a forward model. The inner
skull boundary was segmented out of the MR imaging data sets
and triangulated. The triangle side length was set to 7 mm
(Haueisen et al., 1997).
MEG data preprocessing consisted of artifact rejection, common
mode rejection, band pass filtering (3rd-order Butterworth
20–170 Hz), and baseline correction ( 100 to 0 ms). The noise
estimate was computed separately for each channel as the variance
of the 20% samples with the lowest amplitude. A two-step spatiotemporal dipole localization procedure was performed with
consideration to the time interval of the first cortical components
N20m and P25m. First, a single fixed dipole was fitted in the upstroke of the N20m (time interval from baseline to peak N20m).
This source activity was then projected out for the entire time
interval (comprising N20m and P25m components) and a second
fixed dipole was fitted, which mainly represented the activity of
the P25m component. To verify the found positions, multiple tests
with different starting points were performed using the Nelder–
Mead Simplex method (Nelder and Mead, 1965).
For the sake of comparison, the entire source localization procedure was repeated using the Bz only. As indicated above, Bz was obtained simply by adding the magnetic flux vectors measured by the
three SQUIDs and projecting the sum vector onto the common
device axis.
Source localization was performed with Curry version 4.6 (Compumedics NeuroScan, Charlotte, NC). All other computations were
done in Matlab (The Mathworks, Natick, MA).
3. Results
Fig. 2 shows the butterfly plots of the magnetic signals over
time for the three components Bx, By, and Bz for one volunteer.
The N20m latency, as derived from these plots for all volunteers,
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was 20.3 ± 1.4 ms. The signal-to-noise ratio for all volunteers was
12.8 ± 4.1, 12.7 ± 4.3, and 14.5 ± 5.6 (Bx, By, and Bz). The morphology differs slightly for the three butterfly plots.
Fig. 3 shows an example of the measured magnetic field distributions. The Bz field pattern is similar to the field pattern measured
with standard biomagnetometers and shows a typical dipolar
arrangement for the tangential N20m and a monopolar arrangement for the quasi-radial P25m. For the N20m, the Bx field pattern
shows a slightly quadrupolar arrangement (two negative maxima
in the center of the field pattern) and the By field pattern shows
a tri-polar arrangement. Regarding the P25m, both Bx and By show
dipolar arrangements. This is in agreement with simulated field
patterns (Haueisen et al., 1995). The central points of the field patterns of the N20m and P25m are slightly different, and indicate the
different origins of the two underlying sources. As expected, P25m
quasi-radial activity generally produces lower field amplitudes
(difference in line increment in Fig. 3), which are, however, clearly
above the noise level for all volunteers. Regarding P25m quasi-radial activity in Fig. 3, both Bx and By show higher amplitudes (and
thus higher SNR) than does Bz. Higher SNR generally yields more
stable source localization results.
We also performed a principal component analysis (PCA) for the
interval of the first cortical components N20m and P25m. Because
the two activities are oriented perpendicular to each other, PCA
clearly distinguished the quasi-radial and tangential field patterns.
We calculated the ratio of the eigenvalues as 3.92 ± 0.97 (tangential/quasi-radial), which also corresponds well to the example
amplitude ratio of the measured tangential/quasi-radial field patterns in Fig. 3 (approximately 3.6). Note that the absolute eigenvalues of tangential and quasi-radial field patterns depend on
amplitudes, which cannot be compared across participants because of varying sensor positions.
For 10 of the 11 participants, we found the expected source
locations for both dipoles (N20m and P25m) in the vicinity of the
central sulcus. Fig. 4 shows the results of the source localization
procedure for one volunteer. No reliable localization was obtained
for one participant, which was likely caused by a problem in the
co-registration between MR and MEG coordinate systems. The
mean distance between the quasi-radial and tangential dipoles
was 11.9 ± 5.4 mm, which is within the expected range for the dis-
Fig. 2. Butterfly plots of measured magnetic signals for the three components Bx, By, and Bz for one volunteer (for display purposes, no band-pass filtering was applied). Values
in the time interval 0–13 ms were set to the value at 13 ms to exclude artifacts produced by the electric stimulation.
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Fig. 3. Measured magnetic field distributions of one volunteer for tangential N20m (top row) and quasi-radial P25m (bottom row). The small squares indicate triplet
positions and the small crosses indicate channels omitted because of artifacts (if one channel was omitted, the entire triplet was always switched off). Line increment is 50 fT
in the top row and 20 fT in the bottom row.
Fig. 4. The results of source localization for one volunteer in tilted back view (a)
and tilted left side view (b). The localized tangential (Brodmann area 3b; postcentral wall of the central sulcus; yellow) and quasi-radial (Brodmann area 1;
crown of the post-central gyrus; red) dipoles are indicated by the poles plotted over
the rendered cortical surface (for display purposes, the cortical surface has been
slightly eroded). The positions of the sensors are indicated in blue.
tance between the underlying Brodmann areas 3b and 1. We found
the angle between the two dipoles to be 97.5 ± 28.5°, which is also
in accordance with the expected range.
We additionally performed single component source localization using only the Bz component. As expected, the localization results were generally the same for the N20m. However, only in
three volunteers the single component approach yielded source
locations in the vicinity of the somatosensory system. For the other
seven volunteers, the source locations were in other parts of the
brain. For source localization using only Bz, the mean distance
between the quasi-radial and tangential dipoles was
25.6 ± 14.8 mm, where even the smallest distance was larger than
14 mm.
4. Discussion
In the present experimental study, we demonstrated that it is
possible to localize quasi-radial dipolar activity in the human
somatosensory system using a three-component MEG. The first
cortical activities in Brodmann areas 3b and 1, which can be represented by a tangential and a quasi-radial dipole (Allison et al.,
1991; Buchner et al., 1994; Wood et al., 1985) and which overlap
in time, were clearly distinguished in principal component analysis, dipole location, and dipole orientation.
The findings of the present study are in line with those of previous studies that demonstrated that magnetic field distribution
measured tangentially to the scalp can provide additional information for the solution of inverse problems with multiple sources in
the primary and secondary somatosensory cortex overlapping in
time, after median nerve stimulation (Kim et al., 2003) or finger
stimulation (Kim et al., 2006). Similarly, the usefulness of vectorial
magnetic field measurements was previously shown for discriminating multiple sources of magnetic alpha waves overlapping in
time (Kim and Uchikawa, 2002). In a different field of application,
Bradshaw et al. (1999) suggested that gastric and intestinal activity
can be distinguished based on vectorial magnetic field
measurements and that in general, vectorial measurements
increase the ability to separate different physiological signal
components, as well as non-physiological components.
In the non-invasive diagnosis of spinal cord function for orthopedic and neurologic applications, SQUID vector gradiometers provide more information on the evoked magnetic field distribution in
the spatially limited area of the neck (Adachi et al., 2009). It was
reported that in magnetocardiography, localization of the accessory conduction pathway in a patient with Wolff–Parkinson–
White syndrome was improved when using vector data compared
with one-component field data (De Mehlis et al., 2010). Similarly,
in simulation studies, improved localization accuracy was shown
for single dipoles when using vector data compared with one-component field data (Arturi et al., 2004; Nara et al., 2007). The
improvement can be partly attributed to the higher SNR obtained
by a greater number of sensors. Consequently, with vectorial data,
fewer trials are required in the averaging process in order to
achieve the same localization accuracy (Arturi et al., 2004). A similar result was obtained for distributed sources and minimum
norm solutions (Di Rienzo et al., 2005). On more theoretical
grounds, using a projection method, Di Rienzo and Haueisen
(2007) showed that independent from noise level considerations,
J. Haueisen et al. / Clinical Neurophysiology 123 (2012) 1581–1585
vectorial field data provided more information in the inverse problem compared with that obtained from one-component data.
With regard to the human head, it has been argued that volume
currents have a stronger effect on the tangential components of the
magnetic field (B/, Bh) than on the radial component (Br); accordingly, MEG systems that measure only Br have been suggested.
However, the wide availability of realistic volume conductor models enables volume currents to be taken into account. Moreover,
Kwon et al. (2002), using an auditory stimulation paradigm,
indicated that accurate source locations in the auditory cortex
could also be obtained by using only the tangential components
of the magnetic field.
The present study has several limitations. Our forward computation model included anatomically realistic individual 1-compartment boundary element models. Although boundary element
models provide a more realistic description of conductivity
distribution in the human head compared with simple spherical
models, they have the intrinsic disadvantage of homogeneous
and isotropic conductivity compartments. Finite Element Method
models enable detailed modeling of inhomogeneous and anisotropic conductivity distributions (Güllmar et al., 2010; Haueisen
et al., 2002). We chose the boundary element approach for the
present study for two reasons: these models are currently in more
common use, and model construction is easier to achieve for compartmental models. Consequently, the influence of inhomogeneous
and anisotropic conductivity distributions on the different field
components remains to be investigated.
A further limitation of our experimental study is that it uses a
measurement system designed for magnetocardiography. The flat
bottom cryostat is not optimal for MEG because there is a larger
distance between the sensors and the head at the periphery of
the sensor array. In addition, the patient position unit in this system consists of a fixed array of coils, which is mechanically more
difficult to fix on the head than on the torso.
5. Conclusion
To the best of our knowledge, this is the first study to reconstruct
quasi-radially oriented dipoles based on vectorial biomagnetic
measurements. We conclude that quasi-radial dipolar activity can
be estimated from such measurements and that greater insight into
brain activity may be obtained using three-component magnetoencephalographic measurements compared with those from standard
magnetoencephalography. Vectorial biomagnetic measurements
further improve the signal-to-noise ratio and thus allow for better
localization of weaker components such as the P25m.
Acknowledgements
This work was supported in part by the Deutsche Forschungsgemeinschaft (DFG Grant Ha 2899/7/8–1) and BMBF Grant
03IP605.
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