Download Exposure to high-field MRI does not affect cognitive function

JOURNAL OF MAGNETIC RESONANCE IMAGING 31:1061–1066 (2010)
Original Research
Exposure to High-Field MRI Does Not Affect
Cognitive Function
Marc Schlamann, MD,1* Melanie A. Voigt, MD,1 Stefan Maderwald, MS,1,2
Andreas K. Bitz, MS,1,2 Oliver Kraff, MS,1,2 Susanne C. Ladd, MS, MD,1,2
Mark E. Ladd, MS,1,2 Michael Forsting, MD,1 and Hans Wilhelm, MS3
Purpose: To assess potential cognitive deficits under the
influence of static magnetic fields at various field
strengths some studies already exist. These studies were
not focused on attention as the most vulnerable cognitive
function. Additionally, mostly no magnetic resonance
imaging (MRI) sequences were performed.
Materials and Methods: In all, 25 right-handed men
were enrolled in this study. All subjects underwent one
MRI examination of 63 minutes at 1.5 T and one at 7 T
within an interval of 10 to 30 days. The order of the
examinations was randomized. Subjects were referred to
six standardized neuropsychological tests strictly focused
on attention immediately before and after each MRI examination. Differences in neuropsychological variables
between the timepoints before and after each MRI examination were assessed and P-values were calculated
Results: Only six subtests revealed significant differences
between pre- and post-MRI. In these tests the subjects
achieved better results in post-MRI testing than in preMRI testing (P ¼ 0.013–0.032). The other tests revealed
no significant results.
Conclusion: The improvement in post-MRI testing is only
explicable as a result of learning effects. MRI examinations, even in ultrahigh-field scanners, do not seem to
have any persisting influence on the attention networks of
human cognition immediately after exposure.
Key Words: neuropsychology; ultra-high-field
cognition
J. Magn. Reson. Imaging 2010;31:1061–1066.
C 2010 Wiley-Liss, Inc.
V
1
MRI;
Department of Diagnostic and Interventional Radiology and
Neuroradiology, University Hospital Essen, Germany.
2
Erwin L. Hahn Institute for Magnetic Resonance Imaging, University
Duisburg-Essen, Essen, Germany.
3
Department of Neurology, University Hospital Essen, Germany.
*Address reprint requests to: M.S., Department of Diagnostic and
Interventional Radiology and Neuroradiology, University Hospital
Essen, Hufelandstr. 55, 45122 Essen, Germany. E-mail: [email protected]
Received March 21, 2009; Accepted November 20, 2009.
DOI 10.1002/jmri.22065
Published online in Wiley InterScience (www.interscience.wiley.com).
C 2010 Wiley-Liss, Inc.
V
MAGNETIC RESONANCE IMAGING (MRI) has been utilized in medical diagnostics for more than 25 years. In
that period, more than 300 million MRI examinations
have been performed (1), and currently more than
50,000 are performed daily (2). Very few critical incidents have occurred in this time, and these were mostly
caused by nonobservance of common precautions, for
example, examination of patients with implants not
suitable for MRI (3). Generally, MRI is regarded as a
harmless procedure in clinical routine, operating without ionizing radiation and without harmful effects on
the human body when the known precautions such as
prevention of projectile effects are observed.
The increasing dissemination of scanners with field
strengths above 3 T has led to new discussions on possible biological effects and damages caused by stronger
magnetic fields and/or higher absorption inside the
human body of the transmitted electromagnetic radiofrequency (RF) radiation necessary for tissue excitation.
Possible impairment or disturbing events to the
human brain might be reflected in cognitive deficits.
Some studies have already assessed potential cognitive deficits under the influence of static magnetic
fields at various field strengths (4–7). However, MR
sequences (ie, magnetic gradients and high-frequency
electromagnetic fields) were not assessed as part of
most of these studies. Hence, possible effects caused
by the interaction of the static magnetic field, gradient
fields, and RF energy could not be detected. Additionally, the neuropsychological test battery was short
and not focused on the most vulnerable cognitive
function, which is attention (8–11). A few studies have
assessed subtests on attention, among other things,
but here also no imaging sequences were performed
(12–14). One study performed sequences for sodium
imaging at 9.4 T, but the test battery was not strictly
focused on attention (15).
To help close this gap, the aim of the present study
was to evaluate the potential effects of MRI examinations at 1.5 T and 7 T on attention.
MATERIALS AND METHODS
The local Ethics Committee authorized the examinations as part of fundamental research on high-field
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MR. Written informed consent was obtained from all
subjects prior to scanning.
Subjects and Study Protocol
A total of 25 subjects without history of neurological
diseases were enrolled in the study. To assure homogeneity of the sample, only right-handed men aged
between 20 and 45 years (mean 31.2 years) with comparable intelligence were examined: Intelligence was
assessed by means of a short ‘‘paper-and-pencil’’ test
(Multiple Choice Vocabulary Intelligence Test). The
hereby determined IQ ranged from 104 to 145 (mean
123.3). All subjects had to be native German speakers
to ensure equivalent conditions for the neuropsychological testing.
MR Examination
All 25 subjects underwent one MRI examination at
1.5 T (Magnetom Avanto, Siemens Healthcare, Erlangen, Germany) and one at 7 T (Magnetom 7 T, Siemens Healthcare) with an interval of 10–30 days
(mean 18.1 days). The order of the examinations was
randomized. Twelve subjects were first examined at
1.5 T and 13 started at 7 T.
The cranial MR examination consisted of a fixed variety of spin echo and gradient echo sequences (2D
and 3D) using the standard 12-channel receive-only
matrix head coil at 1.5 T and an 8-channel transmit/
receive head coil (Rapid Biomedical, Wuerzburg,
Germany) at 7 T. The sequences at 1.5 T and at 7 T
were comparable with respect to maximum gradient
strength and gradient slope. The whole-body specific
absorption rate (SAR), which was averaged over the
entire scan time and all participating subjects,
amounted to 0.173 W/kg. This is 8.64% of the corresponding limit in ‘‘normal mode’’ (2 W/kg) or 4.32% of
the limit in ‘‘first-level mode’’ (4 W/kg). At 7 T, fewer
slices were acquired in the same time to compensate
for the higher energy absorption in human tissue at
300 MHz. More relevant might be the local SAR distribution in the head. This information would only be
accessible through numerical simulations in dedicated models of each individual head, so that it is not
available for this study.
All subjects underwent MRI examinations of 63
minutes, one at 1.5 T and one at 7 T in the supine
position. The subjects were contacted repeatedly during the MR examination to avoid falling asleep.
Neuropsychological Testing
Study participants were referred to standardized neuropsychological tests immediately before and after
each MRI examination in a separate room outside the
scanner and control rooms. In total, four neuropsychological examinations were performed in each
subject.
Because of the presumed volatility of possible
effects, neuropsychological testing was strictly
focused on attention. Due to the widespread active
neuronal networks that are involved in attention, this
Schlamann et al.
is considered to be the most vulnerable cognitive
function (8–11). A well-validated set of six standardized psychometric tests was performed. Two paperand-pencil tests were followed by four tests at the
computer using TAP 2.1 software (Test for Attentional
Performance, Psytest Psychologische Testsysteme,
Herzogenrath, Germany). All tests were monitored by
the same experienced neuropsychologist. To minimize
learning effects, a prestudy training session was held
in which the complete test battery was explained and
practiced once before the actual measurements were
obtained.
Paper-and-Pencil Tests
To measure the subjects’ attention and psychomotor
speed, Reitan’s Trail Making Test version B (TMT-B)
was performed. Reitan’s Trail Making Test version A
(TMT-A) was used to measure the rate of information
processing, psychomotor tracking speed, and handeye coordination. In test version A, the task is to connect numbers in a sequence (ie, 1-2-3, etc.) by drawing a line as quickly as possible; in test version B, test
numbers and letters have to be connected (eg, 1A-2B3C, etc.). The corresponding time was measured by a
stopwatch and recorded.
Computer-Based Tests
The test ‘‘Working Memory’’ of the TAP software checks
the control of information flow and actualization of information in working memory. There is no clear distinction between processes of selective attention and
‘‘working memory’’ (16). This task requires continuous
control of the information flow through short-term
memory by presenting numbers on the screen that
must be compared with previously presented numbers. The repetition of a number within a short interval has to be confirmed by pressing a key.
The test ‘‘Flexibility’’ was used to evaluate the orientation flexibility of the focus of attention. Mental flexibility seems to be an important aspect of cognitive
functioning, with the extremes of high distractibility
or flight of ideas on the one side and perseveration or
rigidity on the other. The flexibility of focused attention was tested by a mental alternation between letters and numbers. For testing, two stimuli, one from
each of these symbol sets, were presented simultaneously and randomly on the left or the right side of the
fixation point. In each subsequent presentation, the
target changes from letter to number and back again.
The subject has to press a key as quickly as possible
on the side of the target (left or right) with the corresponding target, either letter or number. Analysis was
performed for the overall test, and subanalysis was
performed for ‘‘change’’ and ‘‘no change’’ of the target
side in comparison to the side of the preceding target.
The test ‘‘Divided Attention’’ was performed to test
the ability of dividing attention and concentrating on
two tasks. Brain-damaged patients frequently report
difficulties in situations where various aspects must
concurrently be paid attention to (17). Divided attention performance can be investigated by executing
Cognitive Function and High-Field MRI
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Table 1
P-values of the Two ‘ Paper-and-Pencil’’ Tests (TMT-A and TMT-B) and the Four Computer-Based Tests (Working Memory, Divided
Attention, Incompatibility, Flexibility), Including Subanalyses
Test
TMT-A 1.5 T
TMT-A 7 T
TMT-B 1.5 T
TMT-B 7 T
Working Memory RT 1.5 T
Working Memory RT 7 T
Divided Attention RT 1.5 T
Divided Attention RT 7 T
Divided Attention RT 1.5 T
Divided Attention RT 7 T
Incompatibility RT 1.5 T
Subtest
P-value
Test
Subtest
P- value
Auditory
Auditory
Visual
Visual
Compatible
0.242
0.065
0.013
0.032
0.689
0.098
0.539
0.572
0.617
0.021
0.946
Incompatibility RT 7 T
Incompatibility RT 1.5 T
Incompatibility RT 7 T
Incompatibility 1.5 T
Incompatibility 7 T
Flexibility RT 1.5 T
Flexibility RT 7 T
Flexibility RT 1.5 T
Flexibility RT 7 T
Flexibility 1.5 T
Flexibility 7 T
Compatible
Incompatible
Incompatible
Overall
Overall
Change
Change
No change
No change
Overall
Overall
0.061
0.778
0.031
0.732
0.024
0.019
0.764
0.128
0.071
0.054
0.948
The results are based on tests for differences in pre-MRI testing vs. post-MRI testing. RT, reaction time.
dual tasks. This is realized by a visual and an auditory task which have to be carried out simultaneously. The visual task consists of crosses that appear
in a random configuration in a 4 4 matrix. The subject has to detect whether the crosses form the corners of a square. The auditory task includes a regular
sequence of high and low beeps. The subject has to
detect an irregularity in the sequence. Analysis was
performed for the auditory and the visual part.
Finally, the test ‘‘Incompatibility’’ was performed to
evaluate the addition of interference through an
incompatibility of stimulus and reaction (‘‘Simon
Effect’’) (18). Arrows pointing to the left or the right
are presented on the left or the right of the fixation
point on the screen. The subject has to press a key on
the side indicated by the direction of the arrow—independent of the position of the arrow. If the side of the
arrow presentation and the side of response are in
concordance, the condition is classified as ‘‘compatible,’’ otherwise as ‘‘incompatible.’’ Subanalysis was
performed for ‘‘compatibility’’ and ‘‘incompatibility.’’
Reaction times and number of failures of each subtest were determined, yielding 22 variables for analysis
in each subject in all neuropsychological sessions.
Statistical Analysis
All analyses were performed using SPSS software
(SPSS 15, Chicago, IL). A P-value below 0.05 was considered to indicate a statistically significant difference.
Differences in neuropsychological variables between
the timepoints before and after each MRI examination
were assessed by use of the Wilcoxon rank test. P-values were calculated and the differences between the
results of the 1.5 T and the 7 T examinations were
calculated.
Before and after the MR examinations the subjects
had to complete a questionnaire on personal state to
exclude malaise or nausea related to the examination
as adulterant factors in neuropsychological testing (19).
RESULTS
None of the subjects reported malaise after the examinations. The interval between the MR examinations of
the 25 subjects at 1.5 T and 7 T ranged from 10–30
days (mean 18.7). Differences in the neuropsychological testing are shown in Table 1 (pre-MRI examination
versus post-MRI examination). The Wilcoxon rank test
revealed no statistically significant differences in most
subtests. P-values varied between 0.013 and 0.948
(Table 2).
Only six subtests revealed significant differences
between pre- and post-MRI. TMT-B revealed P ¼
0.013 at 1.5 T and P ¼ 0.032 at 7 T. The subtest ‘‘Divided Attention, visual’’ revealed a P-value of 0.021 at
7 T, the subtest ‘‘Incompatibility, overall’’ revealed a Pvalue of 0.024 at 7 T, the subtest ‘‘Incompatibility incompatible’’ revealed a P-value of 0.031 at 7 T, and
the subtest ‘‘Flexibility, change reaction time (RT)’’
revealed a P-value of 0.019 at 1.5 T.
Additionally, three borderline cases were noted: TMTA revealed a P-value of 0.065 at 7 T, subtest ‘‘Incompatibility compatible’’ a P-value of 0.061 at 7 T, and subtest
‘‘Flexibility overall ’’ a P-value of 0.054 at 1.5 T.
All cases with statistical significance were related to
improvements in test performance postexposure. Seventeen of 25 subjects (68%) achieved better results in
the TMT-B test following the 1.5 T examinations. Sixteen of 25 subjects (64%) improved in the TMT-B test
following the 7 T examination with respect to the pre7 T test. Seventeen of 25 subjects (68%) improved in
the ‘‘Incompatibility, overall’’ subtest following the 7 T
examination. Seventeen of 25 subjects (68%) had better results in the ‘‘Divided Attention, visual’’ subtest
following the 7 T examinations. Seventeen of 25 subjects (68%) had better results in the ‘‘Incompatibility,
incompatible’’ subtest after 7 T. Nineteen of 25 subjects (76%) had better results in the ‘‘Flexibility,
change’’ subtest after 1.5 T.
DISCUSSION
With the increasing spread of MR scanners with
higher field strengths, the question of possible negative side effects on the human body has moved into
the focus of interest. Patients have reported transient
side effects of MRI examinations such as metallic
taste, vertigo, and dizziness (13,19).
There are three different electromagnetic fields
affecting the body during an MR examination. First,
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Schlamann et al.
Table 2
Standard Deviation and Mean Value of the Subtests
Test
Mean
value
Standard
deviation
Test
Mean
value
Standard
Deviation
TMT-A pre 1.5T
TMT-B pre 1.5T
TMT-A after 1.5T
TMT-B after 1.5T
TMT-A pre 7T
TMT-B pre 7T
TMT - A after 7T
TMT - B after 7T
Working memory RT pre 1.5T
Working memory RT after 1.5T
Working memory RT pre 7T
Working memory RT after 1.5T
Divided attention RT auditory pre 1.5T
Divided attention RT auditory after 1.5T
Divided attention RT auditory pre 7T
Divided attention RT auditory after 7T
Divided attention visual RT pre 1.5T
Divided attention visual RT after 1.5T
Divided attention visual RT pre 7T
Divided attention visual RT after 1.5T
Incompatibility compatible RT pre 1.5T
Incompatibility compatible RT after 1.5T
24.4
48.8
23.2
42.2
24.2
52.8
21.9
45.0
586.9
595.8
591.3
627.2
538.3
541.6
533.0
534.7
721.84
713.56
743.16
711.6
403.8
406.0
4.2
14.4
5.7
9.0
7.3
23.9
6.1
14.9
143.4
145.6
150.8
198.1
82.5
76.5
76.6
69.6
95.7
87.9
97.2
85.2
50.8
55.2
Incompatibility compatible RT pre 7T
Incompatibility compatible RT after 1.5T
Incompatibility incompatible RT pre 1.5T
Incompatibility incompatible RT after 1.5T
Incompatibility incompatible RT pre 7T
Incompatibility incompatible RT after 7T
Incompatibility overall RT pre 1.5T
Incompatibility overall RT after 1.5T
Incompatibility overall RT pre 7T
Incompatibility overall RT after 7T
Flexibility RT change pre 1.5T
Flexibility RT change after 1.5T
Flexibility RT change pre 7T
Flexibility RT change after 7T
Flexibility RT no change pre 1.5T
Flexibility RT no change after 1.5T
Flexibility RT no change pre 7T
Flexibility RT no change after 7T
Flexibility RT overall pre 1.5T
Flexibility RT overall after 1.5T
Flexibility RT overall pre 7T
Flexibility RT overall after 1.5T
415.7
401.7
419.7
418.7
435.1
421.6
410.5
398.0
425.3
411.1
536.7
504.7
533.5
525.8
568.2
542.6
581.8
559.6
557.0
532.3
568.0
550.4
57.9
50.7
58.8
51.7
61.6
53.3
53.5
74.5
57.8
49.8
85.5
100.7
73.3
91.5
107.3
109.4
112.3
97.3
98.6
103.5
97.3
93.5
RT, reaction time/msec.
the static magnetic field is responsible for aligning the
protons of the body, and thus for the number of protons orientated parallel to B0 for imaging. Higher field
strength produces more signal, as the relation
between B0 and the aligned spins is linear.
Second, the gradient magnetic fields with both spatial and temporal variance are responsible for the spatial encoding of the received signal. A well-known fact
is that these gradient magnetic fields can induce neural stimulation (20). Even cardiac stimulation has
been described in animal experiments. These effects
have been observed in studies both with and without
an additional external static magnetic field of 1.5 T
(21,22).
Third, RF pulses excite the signal-emitting protons.
These RF fields generate thermal energy within the
tissue. Studies have demonstrated that examinations
with a whole-body absorption rate of 6 W/kg averaged
over 16 minutes are still tolerated by volunteers (23),
although the clinical limit for ‘‘first-level mode’’ is currently lower at 4 W/kg.
Our study is the first where neuropsychological
testing was combined with the performance of clinical
routine MRI sequences at different field strengths,
including the application of gradient magnetic field
switching and RF exposure in addition to the static
magnetic field. Our results indicate that MRI has no
persisting measurable effects on human cognition, as
attention networks are the most vulnerable parts of
cognition and show no effects after MRI imaging even
at 7 T.
Former Studies
Effects of MRI examinations on the human brain were
demonstrated very early after the introduction of clini-
cal MRI by von Klitzing (24) in 1986. He showed that
auditory evoked potentials were altered in a static
magnetic field of 0.35 T. These alterations normalized
15 minutes after exposure. Hong and Shellock (25)
and Müller and Hotz (26), however, could not confirm
these results. Pacini et al (27) reported that cell cultures of human nerve cells show morphological and
biochemical changes after exposure to a static magnetic field of 0.35 T for 15 minutes. These results
could not be confirmed (28).
In the past several years, several studies involving
neuropsychological testing have been published on
the possible effects of static magnetic fields as well as
low-frequency gradient magnetic fields and radiofrequency fields.
Chakeres et al (4) performed neuropsychological
examinations in 12 women and 13 men after lying in
a static magnetic field of 8 T and 0.05 T. The cognitive
assessment included measures of learning and retention, verbal fluency (spontaneous word generation),
auditory attention, and auditory working memory;
consequently, it was broad-based. The collective was
not homogeneous and no MRI sequences were performed. Hence, possible effects on human cognitive
function caused by synergistic interaction of the static
magnetic field, the gradient fields, and RF energy
could not be evaluated (4). The authors found no significant differences between pre- and postmagnetic
field exposure. Nor were any clinically significant
effects in vital parameters found (6).
Atkinson et al (15) examined 25 volunteers in a 9.4
T system while performing sodium imaging and in a
mock scanner. Before and after the MR examination
the subjects had to undergo a neuropsychological test
battery that contained some subtests on attention. No
effects on cognition were found. This is the only other
Cognitive Function and High-Field MRI
study to date where MR sequences were performed
during the exposure to the static magnetic field. However, the test battery was not strictly focused on attention and the performed sequences are not common in
clinical routine, as sodium imaging is not yet an
established application. No possible effects of the MR
examination were detected.
De Vocht et al (29) examined 20 volunteers blinded
to the exposure situation in the stray field of a 0 T,
1.5 T, and 3 T system. The volunteers performed a
neuropsychological test battery after exposure including tests for the working memory, visual inference,
and eye–hand coordination neurological domains. No
imaging sequences were performed. Nevertheless, de
Vocht et al found some influences on visual and auditory working memory, eye–hand coordination speed,
and visual tracking tasks.
Kangarlu et al (7) examined 10 subjects before and
after resting in a static magnetic field of 8 T for 1
hour. They utilized a Mini-Mental Test and two additional tests to assess language and motor function.
This relatively simple test setting revealed no abnormalities. Likewise, no imaging sequences were performed in that study.
With the exception of one study, all of these publications have in common that no clinical sequences
were performed. Thus, possible synergistic effects of
static and gradient magnetic fields and RF fields
might remain undetected. In some studies the collective was small and heterogeneous, and the neuropsychological testing was not strictly focused on attention. In our study we hypothesized that if there is an
alteration in brain function caused by an MRI examination, a deficit in attention should be detectable.
We also strove to detect any possible interactions
between the different electromagnetic fields to which a
patient is exposed during MRI. For this reason we
performed a complete MRI examination and did not
expose the subjects only to a static magnetic field as,
for example, Chakeres et al (4) chose to do. Any
effects detected in our study would of course have to
be further investigated to determine whether they are
attributable to one of the three fields alone, of if there
are indeed synergistic effects.
Our study demonstrated that MRI examinations at
1.5 T as well as at 7 T do not seem to have any influence on cognition immediately following exposure. No
MR-related effects on attention as the most vulnerable
part of cognition were detectable, although our collective was very homogeneous. Only five of the subtests
revealed significant differences between pre- and
post-MRI exposure, and in each case the difference
was related to an improvement in the test performance post-MRI. Thus, the underlying explanation for
the significance of these subtests is most likely related
to learning effects.
Before and after the MRI examinations, exactly the
same tests were performed. Thus, learning effects are
supported. These learning effects might have been
limited by so-called complementary tests, but preliminary examinations showed that these tests led to
higher scatter in reaction times, so that these tests
were not considered suitable for the number of sub-
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jects in this study. Additionally, no test battery with
four ‘‘complementary’’ tests exists. Usage of a test battery with two ‘‘complementary’’ tests would not be a
sufficient solution. Therefore, we decided to accept a
degree of learning and performed identical tests repetitively. The learning effects between different field
strength exposures were minimized by randomizing
the order of the examinations and by a long time
interval between the MR examinations. Additionally, a
prestudy training session was held in which the complete test battery was explained and practiced once
before the actual measurements were obtained.
Another drawback of this study is that neuropsychological testing was only performed before and after
the MRI examination and not during MR scanning.
Possible transient effects with very fast recovery might
therefore be missed.
In conclusion, despite the mentioned drawbacks,
MRI examinations, even in ultrahigh-field scanners,
do not seem to have any persisting influence on the
attention networks of human cognition immediately
after exposure.
REFERENCES
1. Moller HE, von Cramon DY. Bestandsaufnahme zu Risiken durch
statische Magnetfelder im Zusammenhang mit der UltrahochfeldMRT. Rofo 2008;180:293–301.
2. Schenck JF. Safety of strong, static magnetic fields. J Magn
Reson Imaging 2000;12:2–19.
3. Shellock FG, Crues JV. MR procedures: biologic effects, safety,
and patient care. Radiology 2004;232:635–652.
4. Chakeres DW, Bornstein R, Kangarlu A. Randomized comparison
of cognitive function in humans at 0 and 8 Tesla. J Magn Reson
Imaging 2003;18:342–345.
5. Chakeres DW, de Vocht F. Static magnetic field effects on human
subjects related to magnetic resonance imaging systems. Prog
Biophys Mol Biol 2005;87:255–265.
6. Chakeres DW, Kangarlu A, Boudoulas H, Young DC. Effect of
static magnetic field exposure of up to 8 Tesla on sequential
human vital sign measurements. J Magn Reson Imaging 2003;
18:346–352.
7. Kangarlu A, Burgess RE, Zhu H, et al. Cognitive, cardiac, and
physiological safety studies in ultra high field magnetic resonance
imaging. Magn Reson Imaging 1999;17:1407–1416.
8. Filley CM. The neuroanatomy of attention. Semin Speech Lang
2002;23:89–98.
9. McDowd JM. An overview of attention: behavior and brain. J
Neurol Phys Ther 2007;31:98–103.
10. Raz A. Anatomy of attentional networks. Anat Rec B New Anat
2004;281:21–36.
11. Sturm W, Willmes K. On the functional neuroanatomy of intrinsic
and phasic alertness. Neuroimage 2001;14(1 Pt 2):S76–84.
12. de Vocht F, van-Wendel-de-Joode B, Engels H, Kromhout H. Neurobehavioral effects among subjects exposed to high static and
gradient magnetic fields from a 1.5 Tesla magnetic resonance
imaging system—a case-crossover pilot study. Magn Reson Med
2003;50:670–674.
13. de Vocht F, van Drooge H, Engels H, Kromhout H. Exposure,
health complaints and cognitive performance among employees
of an MRI scanners manufacturing department. J Magn Reson
Imaging 2006;23:197–204.
14. De Vocht F. Gezondheitsklachten en cognitieve effecten door
blootstelling aan magnetische strooivelden van mri-scanners.
Tijdschr Diergeneesk 2007;132:46–47.
15. Atkinson IC, Renteria L, Burd H, Pliskin NH, Thulborn KR. Safety
of human MRI at static fields above the FDA 8 T guideline: sodium
imaging at 9.4 T does not affect vital signs or cognitive ability.
J Magn Reson Imaging 2007;26:1222–1227.
16. Atkinson RC, Shiffrin RM. The control of short-term memory. Sci
Am 1971;225:82–90.
1066
17. van Zomeren AH, van den Burg W. Residual complaints of
patients two years after severe head injury. J Neurol Neurosurg
Psychiatry 1985;48:21–28.
18. Valle-Inclan F, de Labra C, Redondo M. Psychophysiological studies
of unattended information processing. Span J Psychol 2000;3:76–85.
19. Theysohn JM, Maderwald S, Kraff O, Moenninghoff C, Ladd ME,
Ladd SC. Subjective acceptance of 7 Tesla MRI for human imaging. Magma 2008;21:63–72.
20. Schaefer DJ, Bourland JD, Nyenhuis JA. Review of patient safety in
time-varying gradient fields. J Magn Reson Imaging 2000;12:20–29.
21. Bourland JD, Nyenhuis JA, Schaefer DJ. Physiologic effects of
intense MR imaging gradient fields. Neuroimaging Clin N Am
1999;9:363–377.
22. Ham CL, Engels JM, van de Wiel GT, Machielsen A. Peripheral
nerve stimulation during MRI: effects of high gradient amplitudes
and switching rates. J Magn Reson Imaging 1997;7:933–937.
23. Shellock FG, Schaefer DJ, Kanal E. Physiologic responses to an
MR imaging procedure performed at a specific absorption rate of
6.0 W/kg. Radiology 1994;192:865–868.
Schlamann et al.
24. von Klitzing L. Do static magnetic fields of NMR influence biological signals? Clin Phys Physiol Meas 1986;7:157–160.
25. Hong CZ, Shellock FG. Short-term exposure to a 1.5 Tesla static
magnetic field does not affect somato-sensory-evoked potentials
in man. Magn Reson Imaging 1990;8:65–69.
26. Muller S, Hotz M. Human brainstem auditory evoked potentials
(BAEP) before and after MR examinations. Magn Reson Med
1990;16:476–480.
27. Pacini S, Vannelli GB, Barni T, et al. Effect of 0.2 T static magnetic field on human neurons: remodeling and inhibition of signal
transduction without genome instability. Neurosci Lett 1999;267:
185–188.
28. Feychting M. Health effects of static magnetic fields—a review of
the epidemiological evidence. Prog Biophys Mol Biol 2005;87:
241–246.
29. de Vocht F, Stevens T, van Wendel-de-Joode B, Engels H, Kromhout H. Acute neurobehavioral effects of exposure to static magnetic fields: analyses of exposure-response relations. J Magn
Reson Imaging 2006;23:291–297.