Abstract
In utero magnetic resonance imaging (MRI) has significantly increased our knowledge on early fetal brain development. Especially the possibility to expand standard clinical applications of imaging structure to functional imaging has increased the opportunities but also introduced major challenges in the field regarding motion artifacts, group analysis, and generating structural templates. This chapter gives an overview on fetal functional imaging from stimulation to resting-state studies and discusses critical challenges in data analysis. Fetal functional MRI is a powerful approach investigating brain development in utero and has the potential of generating biomarkers for developmental prognosis in the future.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37(1), 90–101. doi:10.1016/j.neuroimage.2007.04.042.
Biswal, B. B. (2012). Resting state fMRI: A personal history. NeuroImage, 62(2), 938–944. doi:10.1016/j.neuroimage.2012.01.090.
Brewerton, L. J., Chari, R. S., Liang, Y., & Bhargava, R. (2005). Fetal lung-to-liver signal intensity ratio at MR imaging: Development of a normal scale and possible role in predicting pulmonary hypoplasia in utero. Radiology, 235(3), 1005–1010.
Brugger, P. C., Stuhr, F., Lindner, C., & Prayer, D. (2006). Methods of fetal MR: Beyond T2-weighted imaging. European Journal of Radiology, 57(2), 172–181.
Chen, Q., & Levine, D. (2001). Fast fetal magnetic resonance imaging techniques. Topics in Magnetic Resonance Imaging, 12(1), 67–79.
De Vries, J. I. P., Visser, G. H. A., & Prechtl, H. F. R. (1982). The emergence of fetal behaviour. I. Qualitative aspects. Early Human Development, 7(4), 301–322. doi:10.1016/0378-3782(82)90033-0.
Derntl, B., Krajnik, J., Kollndorfer, K., Bijak, M., Nemec, U., Leithner, K., …, Schöpf, V. (2015). Stress matters! Psychophysiological and emotional loadings of pregnant women undergoing fetal magnetic resonance imaging. BMC Pregnancy and Childbirth, 15, 25.
Dittrich, E., Kasprian, G., Prayer, D., & Langs, G. (2011). Atlas learning in fetal brain development. Topics in Magnetic Resonance Imaging, 22(3), 107–111.
Dittrich, E., Riklin Raviv, T., Kasprian, G., Donner, R., Brugger, P. C., Prayer, D., et al. (2014). A spatio-temporal latent atlas for semi-supervised learning of fetal brain segmentations and morphological age estimation. Medical Image Analysis, 18(1), 9–21. doi:10.1016/j.media.2013.08.004.
Evans, A. C., Collins, D. L., Mills, S. R., Brown, E. D., Kelly, R. L., & Peters, T. M. (1993). 3D statistical neuroanatomical models from 305 MRI volumes. In 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference (pp. 1813–1817). IEEE. doi:10.1109/NSSMIC.1993.373602.
Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., …, Dale, A. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.
Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346–355.
Fulford, J., Vadeyar, S. H., Dodampahala, S. H., Moore, R. J., Young, P., Baker, P. N., …, Gowland, P. A. (2003). Fetal brain activity in response to a visual stimulus. Human Brain Mapping, 20(4), 239–245.
Fulford, J., Vadeyar, S. H., Dodampahala, S. H., Ong, S., Moore, R. J., Baker, P. N., …, Gowland, P. (2004). Fetal brain activity and hemodynamic response to a vibroacoustic stimulus. Human Brain Mapping, 22(2), 116–121.
Glover, P., Hykin, J., Gowland, P., Wright, J., Johnson, I., & Mansfield, P. (1995). An assessment of the intrauterine sound intensity level during obstetric echo-planar magnetic resonance imaging. British Journal of Radiology, 68(814), 1090–1094.
Gorgolewski, K., Burns, C. D., Madison, C., Clark, D., Halchenko, Y. O., Waskom, M. L., et al. (2011). Nipype: A flexible, lightweight and extensible neuroimaging data processing framework in python. Frontiers in Neuroinformatics, 5, 13. doi:10.3389/fninf.2011.00013.
Habas, P. A., Kim, K., Corbett-Detig, J. M., Rousseau, F., Glenn, O. A., Barkovich, A. J., et al. (2010). A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. NeuroImage, 53(2), 460–470. doi:10.1016/j.neuroimage.2010.06.054.
Hykin, J., Moore, R., Duncan, K., Clare, S., Baker, P., Johnson, I., …, Gowland, P. (1999). Fetal brain activity demonstrated by functional magnetic resonance imaging. Lancet, 354(9179), 645–646.
Jardri, R., Houfflin-Debarge, V., Delion, P., Pruvo, J.-P., Thomas, P., & Pins, D. (2012). Assessing fetal response to maternal speech using a noninvasive functional brain imaging technique. International Journal of Developmental Neuroscience, 30(2), 159–161. doi:10.1016/j.ijdevneu.2011.11.002.
Jardri, R., Pins, D., Houfflin-Debarge, V., Chaffiotte, C., Rocourt, N., Pruvo, J.-P., …, Thomas, P. (2008). Fetal cortical activation to sound at 33 weeks of gestation: A functional MRI study. Neuroimage, 42(1), 10–18.
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841.
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62(2), 782–790. doi:10.1016/j.neuroimage.2011.09.015.
Kanal, E., Gillen, J., Evans, J. A., Savitz, D. A., & Shellock, F. G. (1993). Survey of reproductive health among female MR workers. Radiology, 187(2), 395–399.
Kim, K., Habas, P. A., Rousseau, F., Glenn, O. A., Barkovich, A. J., & Studholme, C. (2010). Intersection based motion correction of multislice MRI for 3-D in utero fetal brain image formation. IEEE Transactions on Medical Imaging, 29(1), 146–158. doi:10.1109/TMI.2009.2030679.
Kok, R. D., de Vries, M. M., Heerschap, A., & van den Berg, P. P. (2004). Absence of harmful effects of magnetic resonance exposure at 1.5 T in utero during the third trimester of pregnancy: A follow-up study. Magnetic Resonance Imaging, 22(6), 851–854.
Krüger, G., & Glover, G. H. (2001). Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magnetic Resonance in Medicine, 46(4), 631–637.
Kuklisova-Murgasova, M., Aljabar, P., Srinivasan, L., Counsell, S. J., Doria, V., Serag, A., …, Rueckert, D. (2011). A dynamic 4D probabilistic atlas of the developing brain. NeuroImage, 54(4), 2750–2763. doi:10.1016/j.neuroimage.2010.10.019.
Lan, L. M., Yamashita, Y., Tang, Y., Sugahara, T., Takahashi, M., Ohba, T., et al. (2000). Normal fetal brain development: MR imaging with a half-Fourier rapid acquisition with relaxation enhancement sequence. Radiology, 215(1), 205–210.
Lowe, M. J. (2012). The emergence of doing “nothing” as a viable paradigm design. NeuroImage, 62(2), 1146–1151. doi:10.1016/j.neuroimage.2012.01.014.
Mailath-Pokorny, M., Kasprian, G., Mitter, C., Schöpf, V., Nemec, U., & Prayer, D. (2012). Magnetic resonance methods in fetal neurology. Seminars in Fetal & Neonatal Medicine, 17(5), 278–284. doi:10.1016/j.siny.2012.06.002.
Moore, R. J., Vadeyar, S., Fulford, J., Tyler, D. J., Gribben, C., Baker, P. N., …, Gowland, P. A. (2001). Antenatal determination of fetal brain activity in response to an acoustic stimulus using functional magnetic resonance imaging. Human Brain Mapping, 12(2), 94–99.
Ogawa, S., Lee, T. M., Kay, A. R., & Tank, D. W. (1990). Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proceedings of the National Academy of Sciences of the United States of America, 87(24), 9868–9872.
Ogawa, S., Tank, D. W., & Menon, R. (1992). Intrinsic signal changes accompanying sensory stimulation: Functional brain mapping resonance imaging. Proceedings of the National Academy of Sciences, 89, 5951–5955.
Raichle, M. E., & Snyder, A. Z. (2007). A default mode of brain function: A brief history of an evolving idea. NeuroImage, 37(4), 1083–1090. doi:10.1016/j.neuroimage.2007.02.041. discussion 1097–9.
Riklin-Raviv, T., Van Leemput, K., Menze, B. H., Wells, W. M., & Golland, P. (2010). Segmentation of image ensembles via latent atlases. Medical Image Analysis, 14(5), 654–665. doi:10.1016/j.media.2010.05.004.
Roche, A. (2011). A four-dimensional registration algorithm with application to joint correction of motion and slice timing in fMRI. IEEE Transactions on Medical Imaging, 30(8), 1546–1554. doi:10.1109/TMI.2011.2131152.
Rosazza, C., Minati, L., Ghielmetti, F., Mandelli, M. L., & Bruzzone, M. G. (2012). Functional connectivity during resting-state functional MR imaging: Study of the correspondence between independent component analysis and region-of-interest-based methods. AJNR. American Journal of Neuroradiology, 33(1), 180–187. doi:10.3174/ajnr.A2733.
Rousseau, F., Oubel, E., Pontabry, J., Schweitzer, M., Studholme, C., Koob, M., et al. (2013). BTK: An open-source toolkit for fetal brain MR image processing. Computer Methods and Programs in Biomedicine, 109(1), 65–73. doi:10.1016/j.cmpb.2012.08.007.
Salimi-Khorshidi, G., Douaud, G., Beckmann, C. F., Glasser, M. F., Griffanti, L., & Smith, S. M. (2014). Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers. NeuroImage, 90, 449–468. doi:10.1016/j.neuroimage.2013.11.046.
Schöpf, V., Dittrich, E., Berger-Kulemann, V., Kasprian, G., Kollndorfer, K., & Prayer, D. (2013). Advanced MRI techniques of the fetal brain. Der Radiologe, 53(2), 136–140. doi:10.1007/s00117-012-2401-5.
Schöpf, V., Kasprian, G., Brugger, P., & Prayer, D. (2012). Watching the fetal brain at “rest”. International Journal of Developmental Neuroscience, 30(1), 11–17.
Schöpf, V., Kasprian, G., Schwindt, J., Kollndorfer, K., & Prayer, D. (2012). Visualization of resting-state networks in utero. Ultrasound in Obstetrics and Gynecology, 39, 487–488.
Schwartz, J. L., & Crooks, L. E. (1982). NMR imaging produces no observable mutations or cytotoxicity in mammalian cells. AJR. American Journal of Roentgenology, 139(3), 583–585.
Serag, A., Aljabar, P., Ball, G., Counsell, S., Boardman, J., Hajnal, J., & Rueckert, D. (2010). Developmental signal intensity changes in subcortical structures of the perinatal brain detected using multi-modal MRI. In MICCAI 2010 Workshop STIA’10 (pp. 1–8).
Seshamani, S., Fogtmann, M., Cheng, X., Thomason, M., Gatenby, C., & Studholme, C. (2013). Cascaded slice to volume registration for moving fetal FMRI. In 2013 IEEE 10th International Symposium on Biomedical Imaging (pp. 796–799). IEEE. doi:10.1109/ISBI.2013.6556595.
Shellock, F. G., & Crues, J. V. (2004). MR procedures: Biologic effects, safety, and patient care. Radiology, 232(3), 635–652. doi:10.1148/radiol.2323030830.
Shellock, F. G., & Kanal, E. (1991). Policies, guidelines, and recommendations for MR imaging safety and patient management. SMRI Safety Committee. Journal of Magnetic Resonance Imaging, 1(1), 97–101.
Smith, F. W., Adam, A. H., & Phillips, W. D. (1983). NMR imaging in pregnancy. Lancet, 1(8314-5), 61–62.
Snyder, A. Z., & Raichle, M. E. (2012). A brief history of the resting state: The Washington University perspective. NeuroImage, 62(2), 902–910. doi:10.1016/j.neuroimage.2012.01.044.
Supino, R., Bottone, M. G., Pellicciari, C., Caserini, C., Bottiroli, G., Belleri, M., et al. (2001). Sinusoidal 50 Hz magnetic fields do not affect structural morphology and proliferation of human cells in vitro. Histology and Histopathology, 16, 719–726.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic Atlas of the human brain: 3-D proportional system: An approach to cerebral imaging. Stuttgart: Thieme Publishers.
Thomason, M. E., Dassanayake, M. T., Shen, S., Katkuri, Y., Alexis, M., Anderson, A. L., …, Romero, R. (2013). Cross-hemispheric functional connectivity in the human fetal brain. Science Translational Medicine, 5(173), 173ra24–173ra24. doi:10.1126/scitranslmed.3004978.
Yamashita, Y., Namimoto, T., Abe, Y., Takahashi, M., Iwamasa, J., Miyazaki, K., et al. (1997). MR imaging of the fetus by a HASTE sequence. AJR. American Journal of Roentgenology, 168(2), 513–519.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Schöpf, V., Langs, G., Jakab, A. (2016). Functional Imaging of the Prenatal Brain. In: Reissland, N., Kisilevsky, B. (eds) Fetal Development. Springer, Cham. https://doi.org/10.1007/978-3-319-22023-9_21
Download citation
DOI: https://doi.org/10.1007/978-3-319-22023-9_21
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-22022-2
Online ISBN: 978-3-319-22023-9
eBook Packages: Behavioral Science and PsychologyBehavioral Science and Psychology (R0)