- Email: [email protected]
Comparison of functional MR-venography and EPI-BOLD fMRI at 1.5 t
Magnetic Resonance Imaging, Vol. 16, No. 8, pp. 989 –991, 1998 © 1998 Elsevier Science Inc. Printed in the USA. All rights reserved. 0730-725X/98 $19.00 1 .00
PII S0730-725X(98)00085-X
● Technical Note
COMPARISON OF FUNCTIONAL MR-VENOGRAPHY AND EPI-BOLD fMRI at 1.5 T KLAUS T. BAUDENDISTEL,* JU¨ RGEN R. REICHENBACH,† ROLAND METZNER,* JOHANNES SCHROEDER,‡ AND LOTHAR R. SCHAD* *Department of Radiology, Deutsches Krebsforschungszentrum (DKFZ) Heidelberg; †Institute of Diagnostic and Interventional Radiology, Friedrich-Schiller-University, Jena; and ‡Department of Psychiatry, University of Heidelberg, Germany Functional magnetic resonance imaging (fMRI) of the brain using blood oxygenation level dependent (BOLD) contrast relies on the changes of paramagnetic deoxyhemoglobin concentration, which affects brain parenchyma and draining venous vessels. These changes in deoxyhemoglobin concentration in venous vessels can also be monitored using a high-resolution susceptibility-based MR-venography technique. Four volunteers participated in the study in which functional MR-venograms were compared with conventional echo-planar imaging (EPI)BOLD-fMRI. In all cases, small venous vessels could be identified close to the areas of activation detected by conventional fMRI. In the venograms, task performance (finger tapping) resulted in a loss of venous vessel contrast compared to the resting state, which is consistent with a local decrease of deoxyhemoglobin concentration. MR-venography allows a direct visualization of the BOLD-effect at high spatial resolution. In combination with conventional fMRI, this technique may help to separate the contribution of brain parenchyma and venous vessels in fMRI studies. © 1998 Elsevier Science Inc. Keywords: Functional MRI; MR-venography; Susceptibility effect; Motor cortex stimulation.
INTRODUCTION
resolution. Because the susceptibility changes during fMRI experiments are not limited to the sites of brain activation, but extend into larger draining venous vessels originating from activated regions, functional venography and fMRI experiments were performed that show a correlation of venous structures and fMRI-BOLD-brain activation at 1.5 T.
Functional magnetic resonance imaging using blood oxygenation level dependent (BOLD-) contrast imaging techniques1,2 relies on the different magnetic properties of oxy- and deoxyhemoglobin. Compared to a resting state, task performance induces a local decrease in the capillary deoxyhemoglobin concentration, which in turn causes a local decrease of blood susceptibility. Apart from functional magnetic resonance imaging (fMRI), the susceptibility effects due to the increased deoxyhemglobin concentration within venous vessels as compared to arteries form the basis for the mapping of venous structures.3 Acquisition of high-resolution, strongly T2*weighted, three-dimensional (3D) MR-data and use of both magnitude and phase information of the complex MR-data offers the possibility to visualize the venous vascular architecture in a 3D projection with high spatial
Imaging was performed on a 1.5-T Siemens VISION whole body MR-system (SIEMENS Medical Systems, Erlangen, Germany) by using a standard circularly polarized head coil. The gradient system equipped with a gradient overdrive is capable of a maximum gradient strength of 25 mT/m with sinusoidal ramps of 330-ms duration.
RECEIVED 2/2/98; ACCEPTED 2/6/98. Address correspondence to Prof. Lothar R. Schad, Forschungsschwerpunkt Radiologische Diagnostik und Therapie,
Deutsches Krebsforschungszentrum (DKFZ). Postfach 101949, D-69120 Heidelberg, Germany. E-mail:[email protected].
MATERIALS AND METHODS
989
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Magnetic Resonance Imaging ● Volume 16, Number 8, 1998
MR-Venography Mapping of the venous structure was performed using a 3D gradient-echo sequence with velocity compensation along each direction. Sequence parameters were: repetition time 5 58 ms, echo time 5 40 ms, flip angle 5 25°, field of view 5 240 mm, slab thickness 5 32 mm, 16 3D-partitions (effective slice thickness 5 2 mm), number of excitations 5 2, acquisition time 5 10 min, 512 readout points, and a reduced number of 320 phaseencoding steps, interpolated to a matrix of 512 3 512. The venograms were reconstructed from magnitude and phase data. A filter mask was derived from the phase data reflecting the phase change due to the susceptibility variation (for details see 3) and multiplied with the magnitude data for selective enhancement of venous vascular structures. Minimum intensity projections of three consecutive slices were calculated after thresholding the data, improving the signal-to-noise ratio. The sequence was acquired both in the resting condition and during task performance. Self-paced finger-tapping movement was used as the activation paradigm. EPI-BOLD-fMRI A free induction decay EPI sequence with sequence parameters: field of view 5 240, thickness 5 3 mm, matrix 5 128 3 128, echo time 5 54 ms, read-out bandwidth of 1470 Hz/pixel was used for the fMRI experiment. Acquisition time for a single image was 130 ms. Twelve consecutive slices were acquired every 3 s.
A fMRI series consisted of 60 images, acquired in cycles of 10 images during rest followed by 10 images during task performance. The same finger tapping paradigm was used as described above. An EPI-BOLD experiment was completed in 3 minutes. Prior to the brain map calculation, motion correction was performed using the MCWAFNI software package.6 Brain activation maps were calculated using an unpaired Student’s t-test. The first two images of each rest/stimulation cycle were excluded from post-processing to avoid corruption of the activation maps due to transient effects. To obtain comparable slice thicknesses as for the venograms, two consecutive t-maps were averaged. Volunteer study. After obtaining written consent, four healthy right-handed volunteers were investigated according to the ethical guidelines of the institution. To minimize head motion, the heads of the volunteers were fixed using adhesive tape segments over the chin and forehead. Following a sagittal scout scan, the venography sequence and the fMRI experiments were performed with a transverse slice orientation. Three consecutive 3D partitions and two consecutive fMRI slices covered the same nominal volume, respectively. The venography sequence was run both in the resting condition and during self-paced finger tapping, followed by the EPI-BOLD experiment. Three volunteers were investigated using right hand task performance; one was investigated using left hand task performance.
Fig. 1. Comparison of functional MR-venograms and EPI-BOLD-fMRI Student’s t-activation map. (a) Venogram obtained in resting condition, and (b) during finger tapping of the left hand. (c) EPI-BOLD-fMRI Student’s t-activation map superimposed on the corresponding anatomical image. Finger tapping of the left hand results in activation of the corresponding sensorimotor cortex and of the supplementary motor area (see arrows). The decreasing deoxyhemoglobin concentration due to brain activation manifests itself in a loss of venous vessel contrast under task performance (see a and b).
Functional MRI using BOLD ● K.T. Baudendistel et al.
RESULTS Figure 1 displays typical venograms and a brain activation image of the slice showing the largest coverage of the sensorimotor cortex and the supplementary motor area. Figure 1a shows the corresponding venogram in the resting condition. In contrast, Fig. 1b shows the venogram obtained during performance of the finger tapping activation paradigm of the left hand. The corresponding fMRI-EPI brain activation map is displayed in Fig. 1c. The Student’s t-activation map was thresholded by a t-value of 2.0 superimposed on the mean value of the corresponding fMRI time series. Left-hand task performance resulted in an increased activation of the corresponding contralateral sensorimotor cortex and the supplementary motor area (Fig. 1c, see arrows). Compared to the resting condition (Fig. 1a), brain activation leads to a decrease in blood deoxyhemoglobin concentration and is consequently reflected in a decreased contrast of the venous vessels in the venogram (Fig.1b). For all subjects, small venous structures could be identified close to the areas of brain activation. DISCUSSION Similar to other previously reported susceptibilitybased methods,4,5 the MR-venography technique makes it possible to directly observe susceptibility changes during brain activation with high spatial resolution. In all cases, small venous vessels could be identified close to the regions of brain activation. Due to the four times lower spatial resolution of the EPI-BOLD fMRI images, the signal contribution originating from the venous vessels cannot be separated from the contribution of brain parenchyma. As has been observed in experiments performed at different field strengths,7,8 the BOLD-effect in capillaries depends roughly quadratic on static field strength, whereas there is a linear dependency for larger vessels. Thus, in contrast to observations at high field (4 T), which facilitate the distinction between capillary and venous contributions, the major part of the observed signal changes at medium and low field strengths may arise from the vascular contribution. Therefore, the inclusion of additional techniques for mapping of vascular vessels may be appropriate for the use of fMRI in clinical routine. Our results indicate a close relationship between the sites of brain activation as detected by BOLD-sensitive EPI-fMRI and the areas of susceptibility changes
991
measured using the venography technique at 1.5 T. The combination of fMRI techniques with functional venography could therefore be an interesting method for separation of signal contributions arising from the vasculature, leaving only the BOLD-effect of the brain parenchyma. Acknowledgment—This work was supported by the Forschungsschwerpunktprogramm, Baden-Wurttemberg, Germany. J.R.R. thanks the RSNA Research and Education Fund for supporting this research through the 1997 RSNA Seed Grant. The authors are grateful to Dr. E. Mark Haacke for several interesting discussions about the technical aspects of the method.
REFERENCES 1. Ogawa, S.; Lee, T.M.; Kay, A.R.; Tank, D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. USA 87:9868 –9872; 1990. 2. Ogawa, S.; Lee, T.M.; Nayak, A.S.; Glynn, P. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 14:68 –78; 1990. 3. Reichenbach, J.R.; Venkatesan, R.; Schillinger, D.J.; Kido, D.K.; Haacke, E.M. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 204:272–277; 1997. 4. Lai, S.; Reichenbach, J.R.; Haacke, M.E. Commutator filter: A novel technique for the identification of structures producing significant inhomogeneities and its application to functional MRI. Magn. Reson. Med. 36:781–787; 1996. 5. Haacke, E.M.; Lai, S.; Reichenbach, J.R.; Kuppusamy K.; Hoogenraad, F.G.C.; Takeichi, H.; Lin, W. In vivo measurement of blood oxygen saturation using magnetic resonance imaging: A direct validation of the blood oxygen level-dependent concept in functional brain imaging. Human Brain Mapping 5:341–346; 1997. 6. Cox, R.W. AFNI. Software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29:162–173; 1996. 7. Turner, R.; Jezzard, P.; Wen, H.; Kwong, K.K.; Le Bihan, D.; Zeffiro, T.; Balaban, R.S. Functional mapping of the human visual cortex at 4 and 1.5 Tesla using deoxygenation contrast EPI. Magn. Reson. Med. 29:277–279; 1993. 8. Ugurbil, K.; Garwood, M.; Ellermann, J.; Hendrich, K.; Hinke, R.; Hu, X.; Kim, S.-G.; Menon, R.; Merkle, H.; Ogawa, S.; Salmi, R. Imaging at high magnetic fields. Initial experiences at 4 T. Magn. Reson. Q. 9:259 –277; 1993.
PII S0730-725X(98)00085-X
● Technical Note
COMPARISON OF FUNCTIONAL MR-VENOGRAPHY AND EPI-BOLD fMRI at 1.5 T KLAUS T. BAUDENDISTEL,* JU¨ RGEN R. REICHENBACH,† ROLAND METZNER,* JOHANNES SCHROEDER,‡ AND LOTHAR R. SCHAD* *Department of Radiology, Deutsches Krebsforschungszentrum (DKFZ) Heidelberg; †Institute of Diagnostic and Interventional Radiology, Friedrich-Schiller-University, Jena; and ‡Department of Psychiatry, University of Heidelberg, Germany Functional magnetic resonance imaging (fMRI) of the brain using blood oxygenation level dependent (BOLD) contrast relies on the changes of paramagnetic deoxyhemoglobin concentration, which affects brain parenchyma and draining venous vessels. These changes in deoxyhemoglobin concentration in venous vessels can also be monitored using a high-resolution susceptibility-based MR-venography technique. Four volunteers participated in the study in which functional MR-venograms were compared with conventional echo-planar imaging (EPI)BOLD-fMRI. In all cases, small venous vessels could be identified close to the areas of activation detected by conventional fMRI. In the venograms, task performance (finger tapping) resulted in a loss of venous vessel contrast compared to the resting state, which is consistent with a local decrease of deoxyhemoglobin concentration. MR-venography allows a direct visualization of the BOLD-effect at high spatial resolution. In combination with conventional fMRI, this technique may help to separate the contribution of brain parenchyma and venous vessels in fMRI studies. © 1998 Elsevier Science Inc. Keywords: Functional MRI; MR-venography; Susceptibility effect; Motor cortex stimulation.
INTRODUCTION
resolution. Because the susceptibility changes during fMRI experiments are not limited to the sites of brain activation, but extend into larger draining venous vessels originating from activated regions, functional venography and fMRI experiments were performed that show a correlation of venous structures and fMRI-BOLD-brain activation at 1.5 T.
Functional magnetic resonance imaging using blood oxygenation level dependent (BOLD-) contrast imaging techniques1,2 relies on the different magnetic properties of oxy- and deoxyhemoglobin. Compared to a resting state, task performance induces a local decrease in the capillary deoxyhemoglobin concentration, which in turn causes a local decrease of blood susceptibility. Apart from functional magnetic resonance imaging (fMRI), the susceptibility effects due to the increased deoxyhemglobin concentration within venous vessels as compared to arteries form the basis for the mapping of venous structures.3 Acquisition of high-resolution, strongly T2*weighted, three-dimensional (3D) MR-data and use of both magnitude and phase information of the complex MR-data offers the possibility to visualize the venous vascular architecture in a 3D projection with high spatial
Imaging was performed on a 1.5-T Siemens VISION whole body MR-system (SIEMENS Medical Systems, Erlangen, Germany) by using a standard circularly polarized head coil. The gradient system equipped with a gradient overdrive is capable of a maximum gradient strength of 25 mT/m with sinusoidal ramps of 330-ms duration.
RECEIVED 2/2/98; ACCEPTED 2/6/98. Address correspondence to Prof. Lothar R. Schad, Forschungsschwerpunkt Radiologische Diagnostik und Therapie,
Deutsches Krebsforschungszentrum (DKFZ). Postfach 101949, D-69120 Heidelberg, Germany. E-mail:[email protected].
MATERIALS AND METHODS
989
990
Magnetic Resonance Imaging ● Volume 16, Number 8, 1998
MR-Venography Mapping of the venous structure was performed using a 3D gradient-echo sequence with velocity compensation along each direction. Sequence parameters were: repetition time 5 58 ms, echo time 5 40 ms, flip angle 5 25°, field of view 5 240 mm, slab thickness 5 32 mm, 16 3D-partitions (effective slice thickness 5 2 mm), number of excitations 5 2, acquisition time 5 10 min, 512 readout points, and a reduced number of 320 phaseencoding steps, interpolated to a matrix of 512 3 512. The venograms were reconstructed from magnitude and phase data. A filter mask was derived from the phase data reflecting the phase change due to the susceptibility variation (for details see 3) and multiplied with the magnitude data for selective enhancement of venous vascular structures. Minimum intensity projections of three consecutive slices were calculated after thresholding the data, improving the signal-to-noise ratio. The sequence was acquired both in the resting condition and during task performance. Self-paced finger-tapping movement was used as the activation paradigm. EPI-BOLD-fMRI A free induction decay EPI sequence with sequence parameters: field of view 5 240, thickness 5 3 mm, matrix 5 128 3 128, echo time 5 54 ms, read-out bandwidth of 1470 Hz/pixel was used for the fMRI experiment. Acquisition time for a single image was 130 ms. Twelve consecutive slices were acquired every 3 s.
A fMRI series consisted of 60 images, acquired in cycles of 10 images during rest followed by 10 images during task performance. The same finger tapping paradigm was used as described above. An EPI-BOLD experiment was completed in 3 minutes. Prior to the brain map calculation, motion correction was performed using the MCWAFNI software package.6 Brain activation maps were calculated using an unpaired Student’s t-test. The first two images of each rest/stimulation cycle were excluded from post-processing to avoid corruption of the activation maps due to transient effects. To obtain comparable slice thicknesses as for the venograms, two consecutive t-maps were averaged. Volunteer study. After obtaining written consent, four healthy right-handed volunteers were investigated according to the ethical guidelines of the institution. To minimize head motion, the heads of the volunteers were fixed using adhesive tape segments over the chin and forehead. Following a sagittal scout scan, the venography sequence and the fMRI experiments were performed with a transverse slice orientation. Three consecutive 3D partitions and two consecutive fMRI slices covered the same nominal volume, respectively. The venography sequence was run both in the resting condition and during self-paced finger tapping, followed by the EPI-BOLD experiment. Three volunteers were investigated using right hand task performance; one was investigated using left hand task performance.
Fig. 1. Comparison of functional MR-venograms and EPI-BOLD-fMRI Student’s t-activation map. (a) Venogram obtained in resting condition, and (b) during finger tapping of the left hand. (c) EPI-BOLD-fMRI Student’s t-activation map superimposed on the corresponding anatomical image. Finger tapping of the left hand results in activation of the corresponding sensorimotor cortex and of the supplementary motor area (see arrows). The decreasing deoxyhemoglobin concentration due to brain activation manifests itself in a loss of venous vessel contrast under task performance (see a and b).
Functional MRI using BOLD ● K.T. Baudendistel et al.
RESULTS Figure 1 displays typical venograms and a brain activation image of the slice showing the largest coverage of the sensorimotor cortex and the supplementary motor area. Figure 1a shows the corresponding venogram in the resting condition. In contrast, Fig. 1b shows the venogram obtained during performance of the finger tapping activation paradigm of the left hand. The corresponding fMRI-EPI brain activation map is displayed in Fig. 1c. The Student’s t-activation map was thresholded by a t-value of 2.0 superimposed on the mean value of the corresponding fMRI time series. Left-hand task performance resulted in an increased activation of the corresponding contralateral sensorimotor cortex and the supplementary motor area (Fig. 1c, see arrows). Compared to the resting condition (Fig. 1a), brain activation leads to a decrease in blood deoxyhemoglobin concentration and is consequently reflected in a decreased contrast of the venous vessels in the venogram (Fig.1b). For all subjects, small venous structures could be identified close to the areas of brain activation. DISCUSSION Similar to other previously reported susceptibilitybased methods,4,5 the MR-venography technique makes it possible to directly observe susceptibility changes during brain activation with high spatial resolution. In all cases, small venous vessels could be identified close to the regions of brain activation. Due to the four times lower spatial resolution of the EPI-BOLD fMRI images, the signal contribution originating from the venous vessels cannot be separated from the contribution of brain parenchyma. As has been observed in experiments performed at different field strengths,7,8 the BOLD-effect in capillaries depends roughly quadratic on static field strength, whereas there is a linear dependency for larger vessels. Thus, in contrast to observations at high field (4 T), which facilitate the distinction between capillary and venous contributions, the major part of the observed signal changes at medium and low field strengths may arise from the vascular contribution. Therefore, the inclusion of additional techniques for mapping of vascular vessels may be appropriate for the use of fMRI in clinical routine. Our results indicate a close relationship between the sites of brain activation as detected by BOLD-sensitive EPI-fMRI and the areas of susceptibility changes
991
measured using the venography technique at 1.5 T. The combination of fMRI techniques with functional venography could therefore be an interesting method for separation of signal contributions arising from the vasculature, leaving only the BOLD-effect of the brain parenchyma. Acknowledgment—This work was supported by the Forschungsschwerpunktprogramm, Baden-Wurttemberg, Germany. J.R.R. thanks the RSNA Research and Education Fund for supporting this research through the 1997 RSNA Seed Grant. The authors are grateful to Dr. E. Mark Haacke for several interesting discussions about the technical aspects of the method.
REFERENCES 1. Ogawa, S.; Lee, T.M.; Kay, A.R.; Tank, D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. USA 87:9868 –9872; 1990. 2. Ogawa, S.; Lee, T.M.; Nayak, A.S.; Glynn, P. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 14:68 –78; 1990. 3. Reichenbach, J.R.; Venkatesan, R.; Schillinger, D.J.; Kido, D.K.; Haacke, E.M. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 204:272–277; 1997. 4. Lai, S.; Reichenbach, J.R.; Haacke, M.E. Commutator filter: A novel technique for the identification of structures producing significant inhomogeneities and its application to functional MRI. Magn. Reson. Med. 36:781–787; 1996. 5. Haacke, E.M.; Lai, S.; Reichenbach, J.R.; Kuppusamy K.; Hoogenraad, F.G.C.; Takeichi, H.; Lin, W. In vivo measurement of blood oxygen saturation using magnetic resonance imaging: A direct validation of the blood oxygen level-dependent concept in functional brain imaging. Human Brain Mapping 5:341–346; 1997. 6. Cox, R.W. AFNI. Software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29:162–173; 1996. 7. Turner, R.; Jezzard, P.; Wen, H.; Kwong, K.K.; Le Bihan, D.; Zeffiro, T.; Balaban, R.S. Functional mapping of the human visual cortex at 4 and 1.5 Tesla using deoxygenation contrast EPI. Magn. Reson. Med. 29:277–279; 1993. 8. Ugurbil, K.; Garwood, M.; Ellermann, J.; Hendrich, K.; Hinke, R.; Hu, X.; Kim, S.-G.; Menon, R.; Merkle, H.; Ogawa, S.; Salmi, R. Imaging at high magnetic fields. Initial experiences at 4 T. Magn. Reson. Q. 9:259 –277; 1993.