Imaging Brain Function in Humans at 7 Tesla
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Magnetic Resonance in Medicine 45:588 –594 (2001)
Imaging Brain Function in Humans at 7 Tesla
Essa Yacoub, Amir Shmuel, Josef Pfeuffer, Pierre-Francois Van De Moortele,
Gregor Adriany, Peter Andersen, J. Thomas Vaughan, Hellmut Merkle, Kamil Ugurbil,
and Xiaoping Hu*
This article describes experimental studies performed to dem- perimental data (10,11,15,16) have consistently revealed
onstrate the feasibility of BOLD fMRI using echo-planar imaging that the specificity, sensitivity, and contrast of the BOLD
(EPI) at 7 T and to characterize the BOLD response in humans response to neural activity increases with the field strength
at this ultrahigh magnetic field. Visual stimulation studies were (also see 17–21). This field strength dependence has led to
performed in normal subjects using high-resolution multishot
a recent surge in the number of high field (3 and 4 T) MRI
EPI sequences. Changes in R2* arising from visual stimulation
systems available. Recently, two human systems operating
were experimentally determined using fMRI measurements ob-
tained at multiple echo times. The results obtained at 7 T were at fields higher than 4 T became available. The 8 T system
compared to those at 4 T. Experimental data indicate that fMRI has generated a great deal of interesting data (22), mostly
can be reliably performed at 7 T and that at this field strength in anatomic imaging. With the 7 T whole-body system in
both the sensitivity and spatial specificity of the BOLD response our laboratory, we have begun experimental fMRI studies
are increased. This study suggests that ultrahigh field MR systems in humans for the first time at magnetic field strengths that
are advantageous for functional mapping in humans. Magn significantly exceed 4 T. The experiments were conducted
Reson Med 45:588 –594, 2001. © 2001 Wiley-Liss, Inc. using a surface coil with a visual stimulation paradigm.
Key words: cerebral function; functional imaging; MRI; fMRI; Functional mapping of the visual cortex using echo-planar
BOLD; ultrahigh field imaging (EPI) at 7 T was demonstrated and activation-
related R *2 changes (⌬R *2 ) were quantified. This article
Since its initial demonstration in 1992 (1–3), functional presents the experimental details and results.
magnetic resonance imaging (fMRI) has evolved into a
widely used methodology for mapping neuronal function.
The basis of most fMRI studies is the blood oxygenation MATERIALS AND METHODS
level dependent (BOLD) contrast (4 – 6), which is derived Data Acquisition
from the fact that the magnetic property of hemoglobin Normal subjects were enrolled for this study, which was
depends on its oxygenation state (7). Because deoxygen- approved by the institutional review board at the Univer-
ated hemoglobin is paramagnetic, deoxygenated blood sity of Minnesota. All subjects provided written consent.
leads to a local decrease in T *2 and T2. Neural activity Functional imaging studies were performed using a visual
causes a local increase in blood flow, which overcompen- stimulation paradigm where the stimulus was generated
sates any increase in oxygenation utilization (8) and leads by red LED goggles flashing at 10 Hz (Grass Instruments,
to a reduction in local deoxyhemoglobin concentration. Quincy, MA). A block design was used for all studies.
Consequently, neural activity leads to an elevation in T2- A 90-cm bore 7 T magnet (Magnex Scientific, Abingdon,
or T *2-weighted images. Based on this principle, the ma- UK) coupled with a Varian INOVA console (Palo Alto, CA)
jority of fMRI experiments are performed by acquiring a was used. For all studies, a quadrature transmit and re-
series of T *2-weighted images while a subject performs a ceive surface coil, designed for covering the occipital cor-
certain task or experiences some type of stimulation. tex (23), was used. Scout images were first obtained with
As a susceptibility phenomenon, the BOLD contrast can an inversion-recovery (IR) prepared TurboFLASH (24) se-
be imaged with MRI at various magnetic field strengths. quence (TI: 1.4 s, TR/TE: 8/3 ms, matrix: 128⫻128, slice
The development of fMRI methodology coincided with the thickness: 5 mm) for identifying the slice of interest. A
introduction of high magnetic fields, and one of the sem- sagittal slice, 6 mm from the midline, was selected. An
inal studies describing fMRI in the human brain for the IR-prepared segmented TurboFLASH (TI: 1.4 s, TR/TE: 8/3
first time was performed at 4 T (1). However, due to their ms, two segments, two averages, matrix: 256⫻256, slice
wide availability, 1.5 T systems are currently used for the thickness: 5 mm) image was obtained over the selected
majority of fMRI studies in humans. In animal models, slice as an anatomic reference. Functional imaging studies
higher magnetic fields (4.7 T and 9.4 T) have been widely were performed using a T *2-weighted EPI sequence. The
used (9 –11). Theoretical considerations (12–14) and ex- EPI sequence was implemented with a readout gradient
consisting of alternating trapezoidal gradient lobes. For
Nyquist ghost removal, a reference scan in the fMRI series
Center for Magnetic Resonance Research and Department of Radiology, was obtained and used to correct for discrepancy between
University of Minnesota, Minneapolis, Minnesota.
the odd and even echoes (25). Note that the algorithm as
Grant sponsor: National Institutes of Health; Grant numbers: P41RR08079 (a
National Centers for Research Resources (NCRR) grant); RO1MH55346; described by Bruder et al. (25) also removes to a large
Grant sponsors: W.M. Keck Foundation; National Foundation for Brain Imag- extent off-resonance induced distortions in the EPI images,
ing (NFFBI). providing a reasonable registration between the fMRI data
*Correspondence to: Xiaoping Hu, Ph.D., CMRR, 2021 6th Street SE, Minne-
apolis, MN 55455. E-mail: xiaoping@cmrr.umn.edu
and the anatomic scan.
Received 12 June 2000; revised 19 September 2000; accepted 16 October fMRI experiments were performed using a segmented
2000. T *2-weighted EPI sequence (matrix: 256⫻256 matrix, eight
© 2001 Wiley-Liss, Inc. 588fMRI at 7 Tesla 589
segments, 20⫻20 cm2 FOV, 5 mm slice, half-Fourier ac- T2 Measurements of Human Venous Blood
quisition with eight additional lines). Due to the relatively
Venous blood was drawn from volunteers from the arm
short T *2 at 7 T, k-space segmentation was needed for
into a standard, evacuated, 10 cc vial that contained an
high-resolution EPI. The EPI images were acquired with a
appropriate amount of solid heparin to prevent clotting.
TR of 0.37 s per segment (corresponding to an acquisition
The tube was quickly wrapped to insulate it and inserted
time per image of 3 s) and an average flip angle of 40°
into a specially constructed RF coil. T2 values were mea-
(averaged over the Calcarine sulcus). During the acquisi- sured with a spin echo sequence with different TEs. Each
tion of fMRI data, the subject’s respiration and heartbeat measurement was performed within a minute and the first
were monitored for subsequent removal of physiological measurement was performed no later than a minute or two
noise. The study was performed in five normal volunteers. after the blood was drawn. The sample tube was then
The fMRI protocol consisted of acquiring 81 images con- removed from the coil, shaken, reinserted, and the mea-
secutively, during which the stimulus was turned off for surement repeated. Three or four such measurements were
nine images and on for nine images in an alternating performed with highly reproducible T2 values in each
manner. The same protocol was run for TEs of 10, 15, 22.5, case. The reported data for each volunteer is the average of
34, and 51 msec. A study was performed in the same group these measurements. Blood O2 saturation was measured
of subjects at 4 T using the same stimulation protocol. The with a blood gas analyzer before and after the T2 measure-
images at 4 T were acquired on the same sagittal slice ments and found to be the same.
using identical parameters except the TEs and a surface
coil based on an equivalent design. The TEs used at 4 T
were 15, 22.5, 34, 51, and 76 msec. At both fields, field RESULTS
homogeneity was optimized with shimming, achieving a
Figure 1a displays activation maps obtained from one sub-
typical slice linewidth of 15 Hz at 4 T and 20 Hz at 7 T.
ject at all TEs for both 7 and 4 T. Similar maps were
generated from data of the other subjects. At the same
Data Processing statistical threshold, the 7 T maps exhibited a considerably
larger activated area at all TEs except the last one, partic-
The acquired k-space data of the T *2-weighted EPI time ularly in the gray matter regions. A paired t-test for the
series were preprocessed using a retrospective technique number of activated pixels (averaged over all TEs) between
(26) to remove physiological fluctuations before the appli- the 7 T and 4 T data showed that the 7 T maps were
cation of a Fourier transform to convert the raw data into significantly (P ⬍ 0.008) larger than those of the 4 T data.
images. The first seven images in each time series were To illustrate the quality of the functional data, the time
discarded to avoid intensity variations during the transi- course of the activated regions are shown for TE of 22 msec
tion to steady state. The four epochs in the fMRI time at 7 T and compared with that of TE of 30 msec at 4 T in
series were averaged to generate a single epoch for further Fig. 1b. Activation correlated changes exhibit a higher
analysis. CNR at 7 T. As expected, the activation maps in Fig. 1a
The T *2-weighted EPI images obtained at different TEs varied with TE and became most prominent at a certain
were first analyzed separately using cross-correlation (27) TE, depending on the field strength. This is more clearly
demonstrated in Fig. 2b, which plots the signal change ⌬S
using a correlation template generated by convolving the
(average signal during activation – average signal during
boxcar function of the stimulation paradigm with a hemo-
rest) as a function of TE for gray matter and vessel ROIs
dynamic response described by Friston et al. (28). Cross-
indicated in Fig. 2a. In the gray matter, ⌬S had a maximum
correlation maps were thresholded with a single threshold
at a TE of 25 msec at 7 T, and 35 msec at 4 T, consistent
(0.7; P ⬍ 0.001) to generate maps at corresponding TEs. In
with the theoretical prediction that there is a maximum for
the second part of the data analysis, regions of interest
activation-induced signal change which occurs when
(ROIs) over gray matter and draining veins, detectable at
TE ⫽ T *2 (29). At 4 T, ⌬S in regions associated with vessels
the image resolution employed, were identified. Veins showed an approximate plateau that persisted until a TE of
were recognized from the anatomic image and the T *2- 35 msec. In the ROI surrounding large vessels, a mono-
weighted images in which they appeared dark (5,15). The tonic decrease was seen with the TE values of 10 msec or
ROIs for the two field strengths were matched by selecting more employed in the 7 T experiments; presumably, this is
the same sagittal slice for the studies at both fields and because the venous blood T *2 is 10 msec or less at 7 T,
using anatomic landmarks for the location of the ROIs (see consistent with the rapid decrease in venous blood T2 and
Fig. 2a). Within each ROI, the average intensity for the T *2 with increasing magnetic field (11). The shortened ve-
activation period, defined as the average of images 4 –9 in nous blood T *2 at the higher magnetic field is also evident
the nine-image stimulation period (the first three images in the T *2-weighted images (Fig. 2a); the large venous ves-
skipped to account for hemodynamic response), and that sel contributions (see arrow in Fig. 1a) disappeared in the
for the resting period, defined to be the average of the three 7 T activation maps at long TEs, while the same vascular
images prior to stimulus onset, were calculated. The T *2 for contributions remained prominent with increasing TE at
the resting and active conditions were derived using ex- 4 T.
ponential fitting of the average image intensity vs. TE. The Figure 3 plots the logarithm of the signal with respect
⌬R *2 of these ROIs was calculated for the two field to TE during rest and activation, respectively. Although
strengths and all subjects. the signals mostly follow an exponential decay, this590 Yacoub et al. FIG. 1. a: Activation maps obtained at different TEs in one subject at 4 T (top) and 7 T (bottom). TEs in msec are marked in the maps. b: Timecourses for TE of 22 msec at 7 T (left) and TE of 34 msec at 4 T (right). exponential behavior is not so well maintained by the was found to be 12.8 ⫾ 0.9 msec at 7 T and 23.5 ⫾ 2.7 msec signals from large blood vessel regions. This is most at 4 T. However, these values can be regarded as approx- likely due to the fact that there is more signal fluctuation imations because of complications associated with partial in the vascular area from cardiac pulsation. In addition, volume effects with surrounding tissue. A separate mea- pixels that contain both tissue and relatively large ve- surement of ex vivo venous blood found the T2 to be nous blood volume fraction (e.g., due to the presence of approximately 7 msec for blood with a normal O2 satura- large blood vessels) may also exhibit an oscillatory be- tion (Y) of 60% (subject 1: T2 ⫽ 6.8 ⫾ 0.4 msec, Y ⫽ 38%; havior (17–20). This oscillatory behavior arises because subject 2: T2 ⫽ 7.1 ⫾ 0.7 msec, Y ⫽ 39%; subject 3: T2 ⫽ the deoxyhemoglobin containing blood has a different 13.1 ⫾ 0.2 msec, Y ⫽ 59%). resonance frequency compared to surrounding tissue Table 1 lists the ⌬R *2 for ROIs in gray matter and venous (17–20). vessel regions for each subject at both field strengths. For The T *2 during the rest condition for the ROIs considered gray matter, the average ⌬R *2 was found to be 1.5 ⫾ 0.3 s⫺1 were as follows. Averaged over all subjects and all resting at 7 T and 0.68 ⫾ 0.09 s⫺1 at 4 T. The ratio between the period images, the gray matter T *2 was 25.1 ⫾ 3.5 msec at ⌬R *2 changes at the two fields is 2.1 ⫾ 0.2, which repre- 7 T and 41.4 ⫾ 5.5 msec at 4 T. Note that this measurement sents a supralinear increase with the field strength. The should be minimally affected by the shimming because vessel ROI (Table 1) at 4 T shows a larger intersubject they are voxel-specific and the linewidth of each voxel variation than the gray matter ROI, presumably due to should be negligible compared to the T *2. These measured more contributions from the vascular signal at 4 T. In the values are in good agreement with the optimum TEs cor- vessel ROI, the ⌬R *2 change increased only slightly with responding to the largest ⌬S. In the vessel regions, the T *2 the field strength.
fMRI at 7 Tesla 591
FIG. 3. a: Plot of signal intensity vs. TE for gray matter ROI and
vessel ROI at 7 T. b: Plot of signal intensity vs. TE for gray matter
ROI and vessel ROI at 4 T.
DISCUSSION
Functional mapping in the visual cortex in humans at 7 T
is demonstrated in this work. Experimental results indi-
cate that fMRI can be robustly performed at 7 T using
ultrafast imaging techniques such as EPI. The study based
on multiple TEs reveals that at 7 T, in the human visual
cortex, T *2 is 25 msec and that this is also the optimal TE
to be used in BOLD based fMRI studies.
Despite the concerns with the high magnetic field, the
only side effect reported by the subjects was a slight diz-
ziness if they were pushed into the magnet too fast. This
effect is similar to what has been reported at 4 T. Prior to
the present fMRI study, we have conducted a behavior
study at 7 T using a mental rotation paradigm that was
previously employed to evaluate the effects of 4 T (30).
The behavior data (to be reported separately elsewhere)
showed that there was no difference in subject perfor-
mance in and outside the magnet.
The studies presented here demonstrate that blood-
related mechanisms that contribute to the BOLD effect
(see discussion in 17–21) are virtually inoperative at 7 T
for TEs equal to or exceeding the optimum TE of
25 msec, while they are still significant at the optimum
TE of 35 msec at 4 T (see Fig. 2, 34 msec and 22 msec
images for 4T and 7T, respectively). This has significant
FIG. 2. a: ROIs for data (4 T: top; 7 T: bottom) shown in Figs. 3b, 2b, implications with respect to the specificity of the func-
and 4. The gray matter ROI is shown in blue and vessel regions are tional images at 7 T since such blood-related effects are
indicated in green. b: Plots of ⌬S vs. TE for gray matter ROI (top) and mostly associated with large blood vessels. Previous
vessel ROI (bottom). studies (13,17–21,31,32) based on eliminating blood
contributions to BOLD mechanism using Stejskal-Tan-592 Yacoub et al.
Table 1
R2* Change Arising From Visual Stimulation
Gray matter ⌬R2* (s⫺1) Vessel region ⌬R2* (s⫺1)
Subject 4 T ⌬R2* 7 T ⌬R2* 4 T ⌬R2* 7 T ⌬R2*
Ratio Ratio
(s⫺1) (s⫺1) (s⫺1) (s⫺1)
kb 0.69 1.5 2.20 1.5 1.9 1.27
sc 0.68 1.4 1.99 1.1 1.3 1.18
pa 0.58 1.0 1.80 1.6 1.7 1.06
rg 0.62 1.4 2.30 1.2 1.3 1.22
dc 0.82 1.9 2.34 0.9 1.1 1.16
Mean ⫾ STD 0.68 ⫾ 0.09 1.46 ⫾ 0.32 2.13 ⫾ 0.23 1.26 ⫾ 0.29 1.46 ⫾ 0.33 1.18 ⫾ 0.09
The negative sign in front of the ⌬R2* is ignored for clarity.
ner gradients (33) have demonstrated that most if not all If only the extravascular BOLD effect associated with
of the signal changes induced by neuronal activation blood vessels larger than capillaries and postcapillary
originate from intravascular or blood-related effects at venules were to dominate the fMRI signals at 4 and 7 T,
1.5 T. The same conclusion was shown to be applicable, then at best only a linear increase in activation related
albeit to a lesser extent, even to 4 T at TE values of ⌬R *2 is expected. If we consider the blood-related contri-
20 –30 msec that are often used at this field strength butions to T *2-weighted fMRI, then the linear dependence
(17–20,34). At these field strengths, the fractional BOLD becomes an upper limit in the 4 T to 7 T comparison.
signal changes induced by activation substantially ex- Therefore, the supralinear increase observed in ⌬R *2 in
ceed the ⬃2% microvascular blood volume fraction in going from 4 to 7 T demonstrates the presence of a signif-
the brain (35). Therefore, these blood-related effects are icant microvascular contribution which is expected to
thought to arise from blood within the large vessels (17) contribute supralinearly. Note that, although the anatomic
(i.e., with diameters comparable or larger than voxel landmarks used in ROI placement were clearly identifiable
dimensions) or voxels that are occupied by both tissue on both the 4T and 7T images, and the slices appear to be
and venous blood with comparable partial volumes (i.e., very similar in location, there may be some error in regis-
voxels partially occupied by relatively large blood ves- tering the ROIs across the different scans in an attempt to
sels). The partial volume effect in the latter case can lead assess the field strength dependence.
to large signal modulations with activation due to the Increased microvascular contribution and diminishing
susceptibility-induced difference in the resonance fre- large vessel contribution to fMRI leads to increased spec-
quencies of the two compartments (17–20). We have
ificity at the higher magnetic field of 7 T. It is possible that
previously argued that these mechanisms should rap-
basal signal fluctuations increase at 7 T. This is currently
idly become inoperative at magnetic fields above 4 T
being investigated separately. However, even if enhanced,
(17–20) due to the rapidly decreasing T2 of blood with
such fluctuations will not necessarily degrade fMRI stud-
increasing magnetic field (11) and we have experimen-
ies at 7 T because they can be eliminated by a variety of
tally demonstrated the absence of these mechanisms at
methods (26,37,38). In fact, in this study, where the fluc-
9.4 T (11). Similar results are also expected at 7 T in
tuations associated with respiration and cardiac pulsation
awake human subjects. While the field strength is some-
were removed, the temporal stability of the fMRI time
what lower relative to the animal studies, fractional
series was found to be comparable at the two field
oxyhemoglobin content in venous blood is also signifi-
cantly higher in awake humans relative to anesthetized strengths and a clear gain in contrast-to-noise ratio for
animals (60% vs. ⬃80% in the animal model in the 9.4 T fMRI was demonstrated in going from 4 to 7 T. This point
study (11)). Consistent with these expectations, blood T2 is also illustrated by the timecourses shown in Fig. 1b. In
at 7 T was found to be approximately 7 msec for 60% addition, MR SNR also increases with field strength, as
oxygenation level. This value is in remarkable agree- systematically demonstrated in a recent volume coil study
ment with the value of 6.7 msec predicted from the (39), providing further gains for fMRI studies. Therefore,
model based on 1.5 T data on human blood T2 (36) if a we conclude that major advantages are realized in fMRI
quadratic dependence on magnetic field is assumed. studies of brain function at 7 T.
In the absence of the above-described BOLD mecha- A potential problem at 7 T is the B1 inhomogeneity and
nism related to blood effects, macroscopic venous blood its potential degradation on SNR. While a full investiga-
vessels can only contribute to T*2-weighted images at 7 T tion of this issue is outside the scope of this article, we
through the extravascular BOLD mechanism arising examined the SNR in the acquired images to get an idea on
from static averaging of field gradients around these this issue. The SNR profiles in the raw images along a line
vessels (e.g., see discussions in 17–20,16-19). Such ef- perpendicular to the surface coil were obtained by smooth-
fects, however, are expected to be small at sites distant ing the image profile and dividing by the noise estimated
from the activated tissue because of dilution from ves- from a region outside the brain. The profiles for the two
sels draining inactive areas. Therefore, they are not ex- field strengths are plotted in Fig. 4 for one of the subjects.
pected to be a major source of degradation of specificity Evidently, the SNR at 7 T is higher for most of the ROI but
of the fMRI maps at 7 T. falls off more quickly, probably due to increased dielectricfMRI at 7 Tesla 593
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