Neurology and Neurosurgery

Research Article ISSN: 2631-4339

Improving the spatial resolution of magnetoencephalography

images
Alfonso de Hoyos1, Javier Portillo2, Pilar Marín1,3, Miguel Á García1,4*, Fernando Maestú5,6, Javier Lafuente1,7, Alberto Ferrus8 and Antonio
Hernando1,3
1
Instituto de Magnetismo Aplicado – Universidad Complutense de Madrid, Spain
2
Grupo de Procesado de Datos y Simulación, Escuela Técnica Superior de Ingenieros de Telecomunicación, Universidad Politécnica de Madrid, Spain
3
Departamento de Física de Materiales, Facultad de Física, Universidad Complutense de Madrid, Spain
4
Instituto de Cerámica y Vidrio – Consejo Superior de Investigaciones Científicas, Spain
5
Laboratorio de Neurociencia Cognitiva y Computacional UCM-UPM, Centro de Tecnología Biomédica, Spain
6
CIBER-bbn Networking Centre on Bioengineering, Biomaterials and Nanomedicine
7
Servicio de Radiodiagnóstico del Hospital General Universitario Gregorio Marañón, Spain
8
Instituto Cajal, Consejo Superior de Investigaciones Científicas, Spain

Abstract
Magnetoencephalography (MEG) is a modern physical technique for the study of the brain function that provides the required temporal resolution. On the contrary,
its spatial resolution is limited, and a proper analysis of the experimental data is required to obtain a reliable 3D image of brain activity with good resolution. Recently,
a modification of the commonly used Linearly Constrained Minimum Variance (LCMV) source location method to improve its spatial resolution was proposed. The
improvement consisted in using pre-stimulus signals to estimate the noise, and average location estimators instead of covariance matrix or data at sensors level. Here
we check the validity of the method by comparing its results with those obtained by functional magnetic resonance imaging. The results confirm that the improvement
of the MEG spatial resolution provides reliable images allowing identifying neural activity.

Introduction particular, as the inverse problem has not a unique solution, additional
constrains need to be used. Those constrains determine the resolution
Understanding the brain function and neural activity is probably and reliability of the obtained images [14].
one of the major challenges of biomedicine in the XXI century [1-3]. In
the last decades, an important number of physical techniques to study A reliable method for the analysis of MEG data is the so-called the
brain function have been developed, including electroencephalography Linearly Constrained Minimum Variance (LCMV) source location
(EEG) [4] magnetoencephalography (MEG) [5,6], functional Magnetic method [15]. It is based on the use of a spatial filtering to localize the
Resonance Imaging (fMRI) [7,8], Computerized Tomography (CT) [9] sources of brain electrical activity, minimizing the output power and
or Positron Emission Tomography (PET) [10] among others. normalizing it by using the noise power. The advantage of this method
Despite the fact that the human brain function is still not fully is that no hypothesis about the number of sources is needed, but it uses
understood, there is a wide consensus in the neurosciences community the covariance of the source electrical activity to determine the spatial
that it involves the synchronization of different areas [11]. Therefore, distribution of the sources.
techniques with both, high spatial and temporal resolution, are needed.
In a recent paper [16], an improvement of the LCMV spatial
Unfortunately, none of the abovementioned techniques to study
filtering model was proposed. The proposed upgrading is based in
brain function provides the required resolution in the time and space
domains suitable to follow the neural activity of the human brain. three key modifications: 1) using the pre-stimulus signal to estimate the
noise, 2) to average location estimators instead of covariance matrix or
In particular, MEG allows following the neural activity with data at sensors levels, and 3) the use of a conservative estimation of the
temporal resolution of milliseconds, but the space resolution is limited noise subspace [16]. These modifications yield a better resolution in the
by the fact that measurements are done out of the brain, and it is determination of the spatial distribution of neural activity.
necessary to solve the inverse problem (i.e., determining the sources
from the magnetic field measured out of the brain) to achieve the
current distribution [12,13]. Therefore, the spatial resolution of MEG
is of the order of centimeters. This spatial resolution is fairly larger than *Correspondence to: Miguel Á García, Instituto de Magnetismo Aplicado ,
that achieved with other techniques. Universidad Complutense de Madrid, ADIF, CSIC, Madrid, Spain, E-mail:
[email protected]
Image reconstruction from MEG data is challenging because
it is an indirect technique based on out of the brain measurements. Key words: magnetoencephalography, magnetic resonance imaging, source
Thus, the analysis to obtain a spatial distribution of neural currents location
is complicated, and different approaches and models are used. In Received: July 04, 2018; Accepted: July 23, 2018; Published: July 26, 2018

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 Hoyos A (2018) Improving the spatial resolution of magnetoencephalography images

In order to evaluate the validity of this model and the reliability p-value adjustment is used [], with a p-value of 0.05, with an extent
of the spatial resolution of the images, we here compare the spatial threshold voxel set to 10. 
distribution of neural activity, during a simple and well-established
task (sequential finger tapping), obtained from MEG data using the MEG source localization algorithm
improved LCMV method with the location obtained from fMRI data. Data model
We found a good agreement between the spatial distributions obtained
with both techniques, pointing out the reliability of the improved The source localization algorithm in use for MEG was a modified
LCMV method for the treatment of MEG experimental data. version of LCMV [15,16]. In all cases, signals were pre-filtered with
a Butterworth bandpass filter of order 4, prior to any subsequent
Experimental computations. In the analysis, we considered three frequency bands:
the alpha band [8-13] Hz, and the sub-bands [8-10] Hz and [10-12] Hz.
Four healthy, right handed subjects, all males, 24, 26, 33 and 37
years old, took part in this study. Subjects were asked to perform According to Gross J et al. [28], activation corresponding to finger
continuous flexion and extension movements (tapping), in a flat tapping task is found in the alpha band, and specifically in the [10-12]
surface with all fingers of both hands. The task consisted in tapping for Hz range.
intervals of 60 s followed by a rest interval of 10 s, alternating right and
The LCMV beamformer is based on the concept of spatial filter
left hands up to four repetitions.
[15]. According to this, given a particular data matrix, the time course
The nature of the procedures was explained in depth and all of a signal originated at a particular point can be estimated. It should
individuals signed a consent form. The universities involved, and the be emphasized that the solution to the inverse problem is not unique
Hospital Review Committees gave approval for the study of human [29] and therefore, in order to obtain a solution with some desirable
subjects. properties, some specific constraints must be introduced, that are
described below.
MEG equipment
Location estimator: LCMV
It is known that using arrays of SQUIDs [17] known as MEG
magnetometers, localization of brain electromagnetic activity The LCMV beamformer is constructed by designing a spatial filter
became possible [18], using different approaches such as the Capon that minimizes the filter output corresponding to each location with
beamformer [19,20], and its successors (LCMV, DICS, SAM, MUSIC, the constraint of unity gain, thus avoiding the trivial zero solution of
etc.) [5,15,18,21–25]. the minimization problem, letting the desired signals to pass through
the filter and minimizing contributions from other sources at locations
In our case, measurements were taken with the Elektra Neuromag
different from the scanned one for each filter output. Details can be
Vector View 306 channel MEG equipment at the Laboratorio
obtained from the study of Van Veen BD et al. [15].
de Neurociencia Cognitiva y Computacional (Cognitive and
Computational Neuroscience Laboratory) of the Centro de Tecnología Modifications of the LCMV method
Biomédica (Center for Biomedical Technology) of the UPM, in Madrid,
Spain. This equipment contains a mixture of 204 planar gradiometers The modifications to this basic scheme are: averaging the neural
and 102 magnetometers. Sampling rate was set to 1 KHz. activity index (NAI) across trials [16], averaging the covariance
matrices across trials, or obtaining a single covariance matrix from the
fMRI equipment averaged measurements matrix.
The BOLD-sensitive (Blood Oxygen Level Dependent) Magnetic Let us denote by ni the NAI arranged as a vector (being the NAI at
Resonance images is a modality of functional Magnetic Resonance a particular point a coordinate of this vector) for the i-th trial (being
Imaging (fMRI) consisting in the indirect measurement of the in a trial a repetition of the finger tapping experiment). Then, the final
vivo brain activity, in a non-invasive way. Via specific sequences, the estimator shall be given by the average of this vector in Nt repetitions,
physiological changes that take place during specific mental processes are and thus,
detected, and more specifically, the changes of magnetic susceptibility 1 Nt

due to the disturbance of the oxygenated and deoxygenated blood ratio n=

Nt
∑n
i =1
i

induced by local brain activity [26]. fMRI measurements were taken

with the 1.5 T Philips Intera (Best, Netherlands), equipment of the Another possible modification is to obtain a single covariance
Hospital Gregorio Marañón (Madrid, Spain) with software version matrix from the covariance matrices of each repetition so that
R11. Gradients of 30 mT/m were used with a slew rate of 150 T/m/s. 1 Nt

Acquisition matrix was 64 × 63, and the acquisition sequence was FFE- C ( y) =
Nt
∑ C ( y)
i =1
i

EPI multi-slice with a repetition time (TR) of 3000 ms, echo time (TE)
Finally, if we denote by Mi the measurement matrix corresponding
of 90 msec and an EPI factor of 63. The anatomic images were obtained
to the i-th repetition, an average measurement matrix can be obtained:
with a FFE T1 3D sequence, with a flip angle of 30º, a TR of 2 ms and
a TE of 9.2 ms. Concerning the resolution of the images, 1.0 × 1.0 × 1 Nt
1.0 mm isotropic voxels were used. Parallel acquisition technique was
M ( y) = ∑ M i ( y)
N t i =1
SENSE x2 with a 6-channel head skull coil. from which a corresponding covariance matrix can be calculated.
For the fMRI paradigm, 8 blocks have been used, each containing The final result, an averaged NAI in the first case or a single NAI in
10 scans. The voxel size for the normalization of the functional images the other two cases, shall be obtained. The common criterion to identify
was 3.59 × 3.59 × 4 mm whereas for the structural images it was 1 × 0.94 activated areas should be to consider activation in those regions with
× 0.94 mm. For the statistical T-test a Family-Wise Error rate (FWE) activity in the range 0.95·NAImax - NAImax. However, the use of this

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 Hoyos A (2018) Improving the spatial resolution of magnetoencephalography images

criterion was not feasible due to the high noise level. Therefore, values The results about the stimulus position obtained from MEG and
in the range 0.8·NAImax - NAImax were used to consider an area activated. fMRI in the whole alpha band essentially agree. The neural activity
determined using MEG appears in some cases slightly out of the brain.
A number of modifications were carried out in order to obtain
better estimates, such as using pre-withening transformations, so the This effect is due to the finite size of the voxels used for the analysis,
noise covariance matrix is the one corresponding to white noise (i.e., that, upon the rigid body rotation used to compare fMRI and MEG
N = αI). These prewithening transformations can be carried out via data, results slightly shifted (the transformation is only exact for
Singular Value Decomposition [30], as obtaining the square root of 0-dimensional points) [31]. Therefore, this comparative study provides
these matrices via Cholesky factorization posed significant numerical additional validation about the results of the modified LCMV method
stability problems. with respect to the results presented in [16].

Coordinate systems Noteworthy, for the 10-12 Hz sub-band, the location of the activity
detected by MEG is very similar to that detected by fMRI, as it concerns
Since the set of points in the fMRI space and in the MEG space the activated areas location. However, MEG also indicates that the
are in different coordinate systems, an appropriate transformation 8-10 Hz sub-band shows activity in regions not detected by fMRI. This
matrix must be applied in order to establish a reasonable comparison activity in the 8-10 Hz sub-band could be explained by the existence
between both techniques. If we consider that voxel sizes may differ also,
of collateral activity that could be assigned to lateral inhibitory
a further transformation is needed. Thus, a Rigid Body Transformation
mechanisms. Note that this lateral activity is well detected by MEG,
[31] was applied to the data from both techniques to make them
whereas it becomes rather transparent for fMRI.
comparable. A detailed description of this transformation is presented
as Supplementary Material. Analyzing each subject individually we find that for subject 1,
As a consequence of these transformations, the axial, coronal and the MEG analysis of the 8-10 Hz sub-band shows additional activity
sagittal planes in fMRI and in the anatomic MRI - superimposed MEG located at contra-lateral position with respect to that observed by both
images do not coincide exactly, as they present tilts in some angle or fMRI and MEG for the 10-12 Hz sub-band. In the case of subjects 2
the other, and thus these cuts are obviously different. However, using and 3, new significant components are observed by MEG in the 8-10
anatomical landmarks as reference this effect can be compensated. Hz sub-band around the components detected in the 10-12 Hz sub-
band by both techniques. It is interesting to note that for subject 3, the
Results and discussion location of the activity associated with 8-10 Hz sub-band corresponds
Table 1 details the NAI maxima obtained from the analysis of the to both sides of the region activated in the 10-12 Hz sub-band. Finally,
MEG data, while table 2 shows the average over for the ensemble of the for subject 4, we can observe that the activated area corresponding to
subjects for each frequency band. the 10-12 Hz sub-band, also observed by both techniques, spreads over
a wider region for the 8-10 Hz sub-band, as analyzed by MEG.
The NAI values are similar for all the subjects. The highest NAI
was observed in the [10-12] Hz sub-band except for S1 where NAI at These results suggest that the data from MEG measurements
the [10-12] Hz frequency sub-band is somewhat smaller than the one corresponding to the whole alpha band represent a mixture of different
observed at [8-10] Hz. contributions and thus, a proper analysis requires separating the data
Figures 1 to 4 present the results of the spatial distribution of neural by sub-bands. Doing so, we find that the activity in the 10-12 Hz sub-
activity obtained from MEG and fMRI. A false color scale has been band essentially agrees with the results previously reported [28], due to
used to indicate the intensity of the detected neural activity, being the the activation of neural circuits of contralateral primary motor cortex
NAI maxima those included in table 1 and NAI minima the 80% on the by the finger tapping activity. On the contrary, the analysis in the 8-10
NAI maxima according to the criterion above described. Each figure Hz sub-band strongly suggests neural activity in adjacent zones, or in
corresponds to a different subject, showing the results of the fMRI, some cases, even separated from the zones activated in the 10-12 Hz
followed by the results of the full alpha band, the results filtered in the sub-band. It should be noted that the activity in the 8-10 Hz sub-band
8-10 Hz sub-band and, finally, the results in the 10-12 Hz sub-band. has NAI values comparable to those in the 10-12 Hz sub-band. We
The fMRI images should be taken as a reference of the stimuli position, argue that the MEG detected activity that extends beyond the fMRI
taking into account that fMRI has high spatial but static resolution. identified domain must correspond to physiological processes that do
Since fMRI and MEG in the same figure may correspond to slightly not rely on sufficiently increased blood flow to be detected by fMRI.
different planes (as above explained), crossmarks indicate identical We consider that functional inhibition of neighboring neurons is the
spatial points determined using anatomical landmarks.
most plausible interpretation. Precedents of the biological relevance
Table 1. NAI maxima for each subject and frequency band of lateral inhibition in perception coherence have been documented
NAImax
extensively in the visual cortex [32] and the prefrontal cortex [33]. The
Frequency band (Hz)
S1 S2 S3 S4 later report actually used MEG analysis of a goal directed motor task
α-band (10-13) 0.411 0.650 0.649 0.621 (inhibition of saccadic eye movement). The actual mechanism of this
8-10 0.354 0.347 0.322 0.360 lateral inhibition, however, remains to be elucidated and future studies
10-12 0.333 0.389 0.378 0.382 should include the potential role of the glia in this effect. Certainly,
electric inhibition is a standard possibility although it requires pre-
Table 2. Averaged NAI maxima across all subjects and frequency band established connectivity and this requirement may possibly reduce
Frequency band (Hz) NAImax plasticity. Alternatively, diffusible neurotransmitters could provide a
α-band (10-13) (5.8 ± 0.6) 10-1 fast, non-restrained, generation of a task-oriented functional network.
8-10 (3.5 ± 0.1) 10-1 Neurotransmitters of this type include NO and protons as described in
10-12 (3.7 ± 0.1) 10-1 the olfactory and visual sensory systems, respectively [34,35].

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 Hoyos A (2018) Improving the spatial resolution of magnetoencephalography images

fMRI

MEG α-band
NAI max

MEG 8 – 10 Hz
sub-band
NAI min

MEG 10 – 12 Hz
sub-band

XZ plane YZ plane XY plane

Figure 1. Spatial distribution of neural activity from fMRI and MEG data in three different planes for subject 1. Crossmarks correspond to the same spatial location determined from
anatomical landmarks. Right Color bar indicates the scale for neural activity (NAI min = 80% NAI max).

fMRI

MEG α-band
NAI max

MEG 8 – 10 Hz
sub-band
NAI min

MEG 10 – 12 Hz
sub-band

XZ plane YZ plane XY plane

Figure 2. Spatial distribution of neural activity from fMRI and MEG data in three different planes for subject 2. Crossmarks correspond to the same spatial location determined from
anatomical landmarks. Right Color bar indicates the scale for neural activity (NAI min = 80% NAI max).

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 Hoyos A (2018) Improving the spatial resolution of magnetoencephalography images

fMRI

MEG α-band
NAI max

MEG 8 – 10 Hz
sub-band
NAI min

MEG 10 – 12 Hz
sub-band

XZ plane YZ plane XY plane

Figure 3. Spatial distribution of neural activity from fMRI and MEG data in three different planes for subject 3. Crossmarks correspond to the same spatial location determined from
anatomical landmarks. Right Color bar indicates the scale for neural activity (NAI min = 80% NAI max).

fMRI

MEG α-band
NAI max

MEG 8 – 10 Hz
sub-band
NAI min

MEG 10 – 12 Hz
sub-band

XZ plane YZ plane XY plane

Figure 4. Spatial distribution of neural activity from fMRI and MEG data in three different planes for subject 4. Crossmarks correspond to the same spatial location determined from
anatomical landmarks. Right Color bar indicates the scale for neural activity (NAI min = 80% NAI max).

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 Hoyos A (2018) Improving the spatial resolution of magnetoencephalography images

Conclusions 14. Iwaki S, Ueno S (1998) Weighted minimum-norm source estimation of

magnetoencephalography utilizing the temporal information of the measured data. J
Our studies comparing MEG and fMRI data (corresponding to Appl Phys 83: 6441.
sequential finger tapping task) suggest that the improvement of the 15. Van Veen BD, van Drongelen W, Yuchtman M, Suzuki A (1997) Localization of brain
LCMV method for the treatment of the MEG data provides a reliable electrical activity via linearly constrained minimum variance spatial filtering. IEEE
Trans Biomed Eng 44: 867-880. [Crossref]
spatial distribution of the neural activity (besides a better resolution).
In particular, it has been found the possibility of detecting by MEG the 16. de Hoyos A, Portillo J, Portillo I, Marín P, Maestú F, et al. (2012) Comparison and
neuronal lateral activity in the vicinity of the group of neurons that are improvements of LCMV and MUSIC source localization techniques for use in real
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17. Zimmerman JE (1977) SQUID instruments and shielding for low-level magnetic
Nevertheless, our work contains a limited number of experiments measurements. J Appl Phys 48: 702.
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Copyright: ©2018 Hoyos A. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
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