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Volume 17, Number 9,
Issue of May 1, 1997
pp. 3178-3184
Copyright ©1997 Society for Neuroscience
Transcranial Magnetic Stimulation during Positron Emission
Tomography: A New Method for Studying Connectivity of the Human
Cerebral Cortex
Tomá Paus1,
Robert Jech2,
Christopher
J. Thompson1,
Roch Comeau1,
Terry Peters1, and
Alan C. Evans1
1 Montreal Neurological Institute, McGill University,
Montreal, Quebec, Canada H3A 2B4, and 2 Department of
Neurology, First Medical Faculty, Charles University, Prague, Czech
Republic
 ABSTRACT
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- FOOTNOTES
- REFERENCES
ABSTRACT 
We describe a new technique permitting the mapping of neural
connections in the living human brain. The method combines two well
established tools of brain research: transcranial magnetic stimulation
(TMS) and positron emission tomography (PET). We use TMS to
stimulate directly a selected cortical area while simultaneously measuring changes in brain activity, indexed by cerebral blood flow
(CBF), with PET. The exact location of the stimulation site is achieved
by means of frameless stereotaxy. In the first study using this
technique, we found significant positive correlations between CBF and
the number of TMS pulse trains at the stimulation site, namely the left
frontal eye field (FEF) and, most importantly, in the visual cortex of
the superior parietal and medial parieto-occipital regions. The pattern
of these distal effects was consistent with the known anatomic
connectivity of the monkey FEF. We suggest that the combined TMS/PET
technique offers an objective tool for assessing the state of
functional connectivity without requiring the subject to engage in any
specific behavior.
Key words:
TMS;
PET;
FEF;
CBF;
saccades;
connectivity;
visual
cortex
INTRODUCTION
We know a great deal about neural connectivity in
the brains of nonhuman primates but little about connectivity in humans because of the limited repertoire of suitable anatomic techniques (Mesulam, 1979 ). Functional techniques based on the correlational analysis of electroencephalographic (Gevins et al., 1979, 1981, 1989;
Thatcher et al., 1986; Tucker et al., 1986) or cerebral blood flow
(CBF; Alexander and Moeler, 1984; Friston, 1994; McIntosh and
Gonzalez-Lima, 1994; Strother et al., 1995; Friston et al., 1996; Paus
et al., 1996) data are indirect and may not show actual neural
connectivity. The correlational studies suffer a major limitation in
that the engagement of a subject in performing a task confounds the
data being acquired: the observed "coactivations" may reflect
relationships between different components of behavior rather than
connectivity. Here we describe a novel technique that allows an
assessment of neural connectivity to be made directly, without
requiring the subject to engage in any specific behavior. The technique
is based on the concurrent use of transcranial magnetic stimulation,
TMS (Barker et al., 1985; Hallett and Cohen, 1989; Maccabee et al.,
1991; Cracco et al., 1993) and positron emission tomography, PET. The
key principle is that of measuring the effect of a focal TMS-induced
electrical stimulation of one region on activity, indexed by changes in
CBF, elsewhere in the brain. It is interesting to note that a
technique based on tracing the spread of experimentally induced
seizures, namely the strychnine neuronography, was used to study neural
pathways in nonhuman primates before the advent of modern anatomic
track-tracing techniques (Dusser de Barenne and McCulloch, 1936; Bailey
et al., 1943, 1944; Petr et al., 1949; Pribram and MacLean, 1953).
In previous studies with single-photon emission tomography or
functional magnetic resonance imaging (fMRI), a suprathreshold transcranial magnetic (Shaffran et al., 1989; Dressler et al., 1990) or
electric (Brandt et al., 1996) stimulation was shown to increase brain
perfusion in the cortex under the coil or electrode, respectively.
Shaffran et al. (1989) also observed increased perfusion in the
cerebellum during TMS of the primary motor cortex. Furthermore, several
authors have combined TMS and electroencephalography (EEG) to explore
transcallosal (Cracco et al., 1989) and cerebello-frontal (Amassian et
al., 1992) connections. The TMS/PET approach described here has an
advantage over that based on EEG in that it allows us (1) to localize
with great precision the TMS-related change in CBF, and (2) to detect
such changes equally well in cortical and subcortical structures. It
also allows for an immediate integration of the connectivity data into
the ever-growing database of blood flow activation studies.
In this study we stimulated a cortical region involved in the control
of eye movements, namely the frontal eye field (FEF). This choice was
motivated by several factors, including (1) the location of the FEF on
the lateral convexity of the cerebral hemispheres and, therefore,
accessibility to the coil-generated magnetic field; (2) the knowledge
of an averaged, i.e., probabilistic, location of the FEF in the human
brain (Paus, 1996); and (3) the knowledge of the anatomic connectivity
of the FEF in the monkey (Huerta et al., 1987; Leichnetz and Goldberg,
1988; Schall et al., 1995). The results obtained in six healthy
volunteers confirmed the feasibility of our approach in that changes in
CBF were observed in several parts of the visual cortex, far remote
from the stimulation site, during TMS of the FEF.
MATERIALS AND METHODS
Experimental design. In six healthy volunteers, a
figure-eight TMS coil was positioned over the left FEF, and CBF was
measured in six 60 sec 15O-H2O scans acquired
with the CTI/Siemens HR+ tomograph. During the scans the
subjects kept their eyes closed, and white noise [80 dB sound pressure
level (SPL)] was played through insert earphones to mask the
coil-generated clicks. Eye movements were recorded with
electro-oculography. It should be pointed out, however, that we did not
expect to evoke any eye movements in this experiment, because several
previous investigators failed to trigger eye movements by TMS of the
frontal cortex even when high-stimulation intensities were used (cf.
Muri et al., 1991; Wessel et al., 1991). To allow for a correlational
analysis of CBF data, we delivered a different number of TMS pulse
trains in the six scans, namely 5, 10, 15, 20, 25, and 30 pulse trains per scan. The order of scans was randomized.
Subjects. Four female and two male subjects volunteered in
the study after giving written informed consent [age, 28 ± 6.5 (mean ± SD) years]. All subjects but one were right-handed.
Following the safety guidelines for the use of a rapid rate TMS in
normal volunteers (Pascual-Leone et al., 1993), we screened the
subjects for a history of neurological disorders, in particular a
personal and family history of epilepsy. The study was approved by the Research and Ethics Committee of the Montreal Neurological Institute and Hospital.
Transcranial magnetic stimulation (TMS). The Cadwell
high-speed magnetic stimulator and the Cadwell figure-eight coil
(Corticoil, see inset of Fig. 1) were used to
produce a focal stimulation of the cerebral cortex through the skull by
rapid switching of a strong (~1.5 T) magnetic field in the coil
(Cohen et al., 1990; Maccabee et al., 1990). The duration of a single
TMS pulse was 200 µsec; the pulses were delivered in five-pulse
trains of 400 msec duration each (between-pulse interval, 100 msec;
i.e., the stimulation frequency of 10 Hz). A different number of pulse
trains was delivered in six 60 sec scans, namely 5, 10, 15, 20, 25, and 30 pulse trains. The shortest between-train interval was 1500 msec. The
intensity of stimulation was set at 70% of the maximum output of the
stimulator. For the figure-eight coil used in this study, the estimated
volume of stimulated tissue was 20 × 20 × 10 mm, with the
point of maximum stimulation being under the central junction of the
two round coils (Cohen et al., 1990; Maccabee et al., 1990; Wassermann
et al., 1996).
Fig. 1.
The top of the figure shows a
coronal (left) and a sagittal (right)
section through a transmission scan obtained in one subject, superimposed on an MR image of the same subject. The TMS coil can be
seen in the inset. Note the figure-eight shape of the
coil. The bottom of the figure contains
three-dimensional plots of the crystal identification matrix obtained
in the absence of magnetic field (A), during magnetic
stimulation (B), and during the same magnetic
stimulation but with metal shields placed between the coil and the
photo multipliers (C). Note a serious distortion of the
matrix during unshielded exposure to the pulse magnetic field
(B).
[View Larger Version of this Image (75K GIF file)]
Location of the target region and positioning of the TMS coil.
To target the same area in all of our subjects, we developed a new
procedure that takes advantage of the standardized stereotaxic space of
Talairach and Tournoux (1988) and frameless stereotaxy (Peters et al.,
1996). First, a magnetic resonance (MR) image of the subject's brain
is acquired and transformed into the standardized stereotaxic space
with an automatic feature-detection algorithm (Collins et al., 1994);
the MR images (160 contiguous 1-mm-thick sagittal slices) were obtained
from a Philips Gyroscan ACS-II (1.5 T). Second, an average,
probabilistic location of the FEF in the stereotaxic space is derived
through a meta-analysis of previous oculomotor blood flow activation
studies (see below). Third, this location, defined by X,
Y, and Z coordinates, is transformed to the
subject's brain coordinate ("native") space with an inverse version of the native-to-stereotaxic transformation matrix. This procedure allows us to determine where the target region is located in
a given subject and, therefore, where to aim the coil during the
experiment. The final step requires us to position the coil over this
location, now marked on the MR image. This is achieved with the aid of
frameless stereotaxy: with the subject lying on the couch in the
scanner, the subject's head is registered with the MR image and the
coil is placed over the target location. Accurate positional and
angular placement of the coil is achieved by interfacing it to the
computer-linked probe of the frameless stereotaxy unit (Viewing Wand,
ISG Technologies, Mississauga, Ontario, Canada). In this manner the
investigator can view the coil movement relative to the subject's MR
image (Fig. 2). When this location is reached, the coil
is locked in place and the PET session begins.
Fig. 2.
The top of the figure shows the
process of registering the subject's head with the corresponding MR
image. A computer-linked probe is touching the bridge of the nose
(right); the matching location is highlighted by a cross
hair on the MR image (left). The bottom
of the figure shows a location targeted by TMS in this study, i.e., the
left frontal eye field, FEF (left), and
the probe-coil interface used to position the coil over this location
(right). 1, Arm of the
frameless-stereotaxy unit; 2, probe inside the
interface; 3, coil inside the interface.
[View Larger Version of this Image (112K GIF file)]
The average location of the left FEF in the standardized stereotaxic
space (i.e., X =  32, Y = 2,
Z = 46) was derived from nine previous blood flow
activation studies of oculomotor control, with a total of 62 subjects
contributing to the database (Paus, 1996). The figure-eight coil was
positioned over this location so that its anterior-posterior axis was
parallel to the interhemispheric fissure, the handle of the coil was
pointing in the anterior direction (i.e., toward the nose), and the
plane of the coil was tangential to the skull (see Fig. 1,
top).
PET: effect of magnetic field on photo multipliers.
Although the coil-generated field lasts only for 200 µsec and
falls off quickly with distance, it still could affect photo
multipliers and the related electronic circuits housed in the gantry of
the scanner. We have, therefore, tested possible effects of magnetic field on data acquisition in a single detector assembly. For this purpose we used a single-detector assembly from a Scanditronix PC-2048
PET scanner (Evans et al., 1991). The figure eight coil was positioned
19 cm from the photo multipliers. Data were acquired for a period of 10 sec, during which time the Cadwell stimulator was either off or on.
Stimulation parameters were set at a 10 sec continuous train of pulses,
delivered at 10-Hz frequency and with the intensity of 40% of the
maximum output of the stimulator. We also tested the effect of
positioning metal sheets with high magnetic-shielding properties (made
by Magnetic Shield Corporation) between the single-detector assembly
and the coil.
PET: acquisition and analysis of CBF data. In the actual
study, PET scans were obtained with a CTI/Siemens HR+
63-slice tomograph operated in a three-dimensional acquisition mode.
The distribution of CBF was measured during a 60 sec scan by means of
the 15O-labeled H2O bolus method (Raichle et
al., 1983). In each scan 10 mCi of 15O-labeled
H2O was injected in the left antecubital vein. No arterial blood samples were acquired in this study. Because a linear
relationship exists between the activity counts and CBF (Herscovitch et
al., 1983), the count values can be used in the absence of the arterial blood samples as close approximations of CBF values. The CBF images were reconstructed with a 14 mm Hanning filter, normalized for differences in global CBF (henceforth "normalized CBF"),
coregistered with the individual MRIs (Woods et al., 1993), and
transformed into stereotaxic space (Talairach and Tournoux, 1988) by
means of an automated feature-matching algorithm (Collins et al.,
1994).
To protect the photo multipliers in the PET detectors from the effects
of the coil-generated magnetic field, we formed an insert consisting of
four layers of 0.5-mm-thick mu-metal in a cylinder, the outer diameter
of which matched the inner diameter of the scanner's patient port,
namely 63 cm. These sheets are of uniform density and therefore do not
cause any artifacts in the images. They do, however, cause increased
attenuation and result in a 22% loss in coincidence counts when
inserted. A blank transmission scan was performed with the magnetic
shielding in place before the subject was scanned. Without this scan,
the subject's head would appear 22% denser, and this would compromise
both the scatter and attenuation correction.
Once the subject and the coil assembly had been positioned in the
scanner, a 10 min transmission scan was performed. The transmission data were used to correct for attenuation of gamma rays caused by all
the objects in the scanner, including the coil, the coil mount, and the
metal sheets. The transmission scan also permits verification of the
final position of the coil relative to the acquired PET and MR images
(see Fig. 1, top).
To assess the significance of the relationship between the number of
TMS pulse trains and normalized CBF (i.e., their linear regression), we
calculated a number-of-trains regression map. All of the following
calculations were performed for each of the three-dimensional volume
elements (voxels) constituting a volume. The data set consisted of
normalized CBF obtained in six subjects, scanned six times each during
the TMS, yielding a total of 36 CBF volumes. The effect of TMS rate on
CBF was assessed by means of an ANCOVA (Sokal and Rohlf, 1981), with
subjects as a main effect and the number of pulse trains administered
during the scan as a covariate. The subject effect was removed, and the
parameter of interest was the slope of the effect of the number of
pulse trains on normalized CBF. An estimate of the slope,
 S, and its standard deviation,
s, were obtained by a least-squares fit of the
model (ANCOVA) at each voxel. In total, 36 values of the covariate were
used, corresponding to the 36 volumes in the data set. The degrees of
freedom (df) of the estimate of the standard deviation
(s) were increased from 29 (36 - 6 - 1)
by pooling s across all voxels, and this
replaced a voxel s in the denominator of the
t statistic, t = S/pooled s, so that its
distribution was normal. The resulting t statistic map
tested whether, at a given voxel, the slope of the regression was
significantly different from zero; the presence of a significant peak
was tested by a method based on three-dimensional Gaussian random-field
theory, which corrects for the multiple comparisons involved in
searching across a volume (Worsley et al., 1992). Values equal to or
exceeding a criterion of t = 3.5 were considered
significant (p < 0.0004, two-tailed,
uncorrected), yielding a false positive rate of 0.58 in 555 resolution
elements (each of which has dimensions 14 × 14 × 14 mm), if
the brain volume is 1500.00 ccm.
RESULTS
Effects of magnetic field on photo multipliers
Figure 1 (bottom, A-C) shows 16 peaks
corresponding to the 4 × 4 crystal array in the detector block.
Despite the fact that the duty cycle of the magnetic field was only
0.2%, this field caused a serious distortion in the crystal
identification matrix. The extent of the distortion indicated that the
field-related effects went beyond the 200 µsec pulse. These
distortions can be prevented, however, by placing three well grounded
sheets of metal with high magnetic-shielding properties between the
coil and the detector (see Fig. 1, bottom, C).
Behavioral effects of TMS
No eye movements were elicited by the stimulation, nor did the
subjects report any visual or other sensations during the scans. They
could feel "tapping" of the coil on the scalp and, in varying degrees, could hear the clicks. Two subjects noticed differences in the
number of pulse trains delivered in different scans.
Effects of TMS on regional CBF
Figure 3 and Table 1 summarize the
main findings obtained by correlating, on a voxel-by-voxel basis,
normalized CBF with the number of TMS pulse trains. A significant
positive correlation between CBF and the number of pulse trains was
observed in the target region, i.e., the left FEF. Furthermore,
positive covariations also were observed in several areas of the visual
cortex, namely in the left medial parieto-occipital (PO) cortex and in
the left and right superior parietal cortex. In addition, a positive
correlation was found in the right supplementary eye field (SEF)
located on the medial wall of the frontal lobe.
Fig. 3.
Brain regions that showed significant
(t > 3.5) correlations between CBF and the number
of TMS pulse trains. The top of the figure shows a
significant correlation in the vicinity of the frontal eye field
(FEF), i.e., in the stimulated area. The
bottom of the figure shows one of the cortical regions
that most likely was activated through the spread of electrical
stimulation from the FEF, namely the parieto-occipital
(PO) cortex of the ipsilateral hemisphere. A similar
region is known to be connected anatomically with the FEF in the monkey
(Schall et al., 1995).
[View Larger Version of this Image (107K GIF file)]
DISCUSSION
The results of our study demonstrate the feasibility of the
combined TMS/PET approach for revealing neural connectivity in the
living human brain. In the ensuing discussion first we shall address
the issue of locating and targeting a cortical region for a TMS/PET
experiment. Then we will compare our findings with those of previous
blood flow activation studies of oculomotor control and with the
results of anatomic tracing studies performed by others in the
monkey.
Locating and targeting the cortical region-of-interest
In this study we used frameless stereotaxy to aim the coil at the
probabilistic location of the left FEF. In each subject the likelihood
of the FEF being included in the stimulated volume depends on the
following three factors: first, the size of the brain volume stimulated
by the Cadwell Corticoil, which was estimated to be approximately
20 × 20 × 10 mm. The strength of the stimulation field
drops to 50% of the peak at ~10 mm from the peak. Second, the
accuracy of the frameless stereotaxy guiding the coil, which was
evaluated by Zinreich et al. (1993) to vary between ± 2-4 mm.
Third, the accuracy of the probabilistic approach in localizing the
individual's FEF. The latter factor is influenced by the extent of
interindividual and interstudy differences in the FEF location. On the
basis of the data obtained in one of our previous studies of oculomotor
control (Paus et al., 1995), we calculated the 95% confidence
intervals for the X, Y, and Z
coordinates of the left FEF. The coordinates were obtained in nine
individual subjects by subtracting CBF obtained in a baseline scan (no
eye movements) from that obtained during the execution of large
horizontal saccades in darkness. The confidence intervals were 46 to
52 mm (X), 2 to 9 mm (Y), and
48 to 54 mm (Z). Thus, the extent of interindividual variability was limited by a sphere with a 6 mm diameter.
The extent of interstudy variability in the location
of the left FEF, based on the results of nine studies performed in four
different institutions, was of a similar magnitude (see Table 4 in
Paus, 1996). This range of interindividual and interstudy variability indeed supports the rationale of the current approach of PET
activations studies, namely that of using standardized stereotaxic
space and blurred images to register homologous functional units across individuals. Thus, considering the extent of the stimulated volume, the
estimated 6 mm error of the probabilistic approach is unlikely to
introduce significant noise in a given TMS/PET study. Nevertheless, it
is conceivable that future improvements of the focality of TMS or the
design of a particular TMS/PET experiment would justify going beyond
the probabilistic approach and identifying the location of a
region-of-interest in each individual subject. For example, fMRI, or the actual effects of TMS on a specific behavior, can be used to guide the positioning of the coil in a subsequent TMS/PET study.
Connectivity of the human FEF
In this study TMS with the coil positioned over the probabilistic
FEF elicited not only local changes in the cortex under the coil, but,
most importantly, changes in CBF in several cortical regions far
removed from the stimulation site. Although the TMS-induced electric
field excites neurons and/or their axons located within the stimulated
volume in both orthodromic and antidromic directions, the distal
changes in CBF most likely would reflect the former, because mainly the
orthodromic stimulation leads to changes in synaptic activity (Wong and
Moss, 1992). The pattern of the distal effects of the stimulation is
consistent with the results of previous blood flow activation studies
of oculomotor control. For example, we previously observed increases in
CBF in the left superior parietal cortex during the execution of
visually guided eye movements (Paus et al., 1993); these increases were
located within 5-10 mm of those observed in this study. Similarly, the
correlation peak found in the right SEF is located just 6 mm ventral
and 2 mm caudal to those observed in our studies of oculomotor control
(Paus et al., 1993). The previous studies involved an execution of
30-50 saccadic eye movements per scan. As previously mentioned, no
TMS-related eye movements were detected in the present study. Thus, the
observed distal CBF changes should be attributed solely to the spread
of activation from the stimulation site along known anatomic pathways. Such pathways are well known in the monkey brain. In a recent investigation Schall et al. (1995) described anatomic connections between the medial portion of the monkey FEF and several areas of the
dorsal visual stream, including those in the posterior part of the
superior parietal cortex and in the medial parieto-occipital cortex
(PO). In the present study a comparable set of visual areas was
activated by TMS of the left FEF. This degree of consistency between
the anatomic tracing studies of the monkey FEF and the present TMS/PET
study of the human FEF validates this approach to the study of neural
connectivity in the human cerebral cortex. Nevertheless, further
investigations are needed to explore several technical issues,
including the effects of coil orientation, stimulus intensity, and
current direction on the pattern of distal CBF changes. For example, it
has been shown that the tangential and radial coil orientations,
relative to the subject's head, over the frontal cortex elicit
electromyographic responses consistent with preferential activation of
cortico-cortical (I-wave) and cortico-spinal (D-wave) pathways,
respectively (Maccabee et al., 1991). Given the tangential orientation
used in the present study, our finding of CBF changes in the distal
cortical areas and the lack of such changes in subcortical structures
is consistent with the Maccabee et al. (1991) results. It remains to be
seen whether different stimulation protocols preferentially would
activate ipsi- and contralateral cortico-cortical pathways,
respectively, or cortico-subcortical connections, such as those known
to link the FEF with the ipsilateral thalamus and superior colliculus. Furthermore, it should be kept in mind that blood flow changes in small
subcortical structures, such as the individual thalamic nuclei and the
superior colliculus, are difficult to detect even when the subject is
moving his eyes.
Summary and conclusions
Overall, our findings confirm that (1) TMS induces focal changes
in brain activity that, in turn, lead to changes in regional CBF, and
(2) such changes can be observed not only at the stimulation site but,
most importantly, in regions presumably connected with this site. We
believe that the combined TMS/PET technique opens up important new
avenues for in vivo studies of neural connectivity in the
human brain. Besides the mapping of neural connectivity of the cerebral
cortex in healthy volunteers, it also has potential in clinical studies
of various neurological and psychiatric disorders for which it is
crucial to evaluate the state of functional connectivity independent of
the sensory, motor, and cognitive abilities of the patient. For
example, the TMS/PET mapping of fronto-cortical connectivity in
patients with schizophrenia may confirm or put to question the presumed
abnormalities of functional connectivity in this disorder (Friston and
Frith, 1995). The effectiveness and neural mechanisms of treatment
interventions, such as rehabilitative training in stroke victims, also
would be evaluated more effectively if the behavior targeted by the
intervention, such as the extent of residual movement, is not part of
the imaging protocol. Thus, the combined TMS/PET approach offers an
objective tool for assessing the state of functional connectivity in
the living human brain independent of possible behavioral
confounds.
FOOTNOTES
Received Jan. 9, 1997; revised Feb. 11, 1997; accepted Feb. 12, 1997.
This work was supported by the McDonnell-Pew Program in Cognitive
Neuroscience and the Medical Research Council (Canada) Special Project
SP-30. Dr. Jech's stay at the Montreal Neurological Institute (MNI)
was funded by the Granting Agency of the Czech Republic (GACR 0376) and
the Czech Ministry of Health (IGA MZ 35-71-31 and IGA MZ 35-72-3). We
thank the Cadwell laboratories for providing us with the high-speed
magnetic stimulator and for the technical advice of their engineer Mike
Vance. We also thank Bryan Hynes and Mike Mazza from the MNI/Hospital
for building the coil-probe assembly, Regina Visca for her assistance
with various aspects of the project, and the staff of the McConnell
Brain Imaging Center for their highly professional assistance in data
acquisition and preprocessing. We also thank Drs. Brenda Milner and
Robert Zatorre for comments on this manuscript.
Correspondence should be addressed to Dr. Tomá Paus,
Montreal Neurological Institute, 3801 University, Montreal, Quebec, Canada H3A 2B4.
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