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MRI-based localization of electrophysiological recording sites within the cerebral cortex at single-voxel accuracy

Abstract

The localization of microelectrode recording sites in the layers of primate cerebral cortex permits the analysis of relationships between recorded neuronal activities and underlying anatomical connections. We present a magnetic resonance imaging method for precise in vivo localization of cortical recording sites. In this method, the susceptibility-induced effect thickens the appearance of the microelectrode and enhances the detectability of the microelectrode tip, which usually occupies less than a few percent of the volume of an image voxel. In a phantom study, the optimized susceptibility-induced effect allowed tip detection with single-voxel accuracy (in-plane resolution, 50 μm). We applied this method to recording microelectrodes inserted into the brains of macaque monkeys, and localized the microelectrode tip at an in-plane resolution of 150 μm within the cortex of 2–3 mm in thickness. Subsequent histological analyses validated the single-voxel accuracy of the in vivo tip localization. This method opens up a way to investigate information flow during cognitive processes in the brain.

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Figure 1: Development and concept of our MRI-based in vivo localization method.
Figure 2: Effects of B0 angle and frequency encoding direction.
Figure 3: Effects of in-plane resolution and other scan parameters.
Figure 4: Localization of the microelectrode tip within the monkey cortex.
Figure 5: Localization accuracy of the microelectrode tip within the cortex.
Figure 6: Stability of the microelectrode tip position across days on in vivo MR images.

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References

  1. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    CAS  Google Scholar 

  2. Evarts, E.V. A technique for recording activity of subcortical neurons in moving animals. Electroencephalog. Clin. Neurophysiol. 24, 83–86 (1968).

    CAS  Google Scholar 

  3. Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    CAS  Google Scholar 

  4. Andersen, R.A. & Buneo, C.A. Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 25, 189–220 (2002).

    CAS  Google Scholar 

  5. Nakahara, K., Hayashi, T., Konishi, S. & Miyashita, Y. Functional MRI of macaque monkeys performing a cognitive set-shifting task. Science 295, 1532–1536 (2002).

    CAS  Google Scholar 

  6. Douglas, R., Markram, H. & Martin, K. Neocortex. in The Synaptic Organization of the Brain 5th edn. (ed. Shepherd, G.M.) 499–558 (Oxford University Press, New York, 2004).

    Google Scholar 

  7. Suzuki, H. & Azuma, M. A glass-insulated “Elgiloy” microelectrode for recording unit activity in chronic monkey experiments. Electroencephalogr. Clin. Neurophysiol. 41, 93–95 (1976).

    CAS  Google Scholar 

  8. Nahm, F.K., Dale, A.M., Albright, T.D. & Amaral, D.G. In vivo microelectrode localization in the brain of the alert monkey: a combined radiographic and magnetic resonance imaging approach. Exp. Brain Res. 98, 401–411 (1994).

    CAS  Google Scholar 

  9. Fung, S.H., Burstein, D. & Born, R.T. In vivo microelectrode track reconstruction using magnetic resonance imaging. J. Neurosci. Methods 80, 215–224 (1998).

    CAS  Google Scholar 

  10. Glimcher, P.W. et al. Application of neurosonography to experimental physiology. J. Neurosci. Methods 108, 131–144 (2001).

    CAS  Google Scholar 

  11. Jog, M.S. et al. Tetrode technology: advances in implantable hardware, neuroimaging, and data analysis techniques. J. Neurosci. Methods 117, 141–152 (2002).

    CAS  Google Scholar 

  12. Tammer, R. et al. Compatibility of glass-guided recording microelectrodes in the brain stem of squirrel monkeys with high-resolution 3D MRI. J. Neurosci. Methods 153, 221–229 (2006).

    CAS  Google Scholar 

  13. Haacke, E.M., Brown, R.W., Thompson, M.R. & Venkatesan, R. Magnetic Resonance Imaging: Physical Principles and Sequence Design (John Wiley & Sons, New York, 1999).

    Google Scholar 

  14. Aube, C. et al. Magnetic resonance imaging characteristics of six radiofrequency electrodes in a phantom study. J. Vasc. Interv. Radiol. 15, 385–392 (2004).

    Google Scholar 

  15. Bezdek, J.C., Hall, L.O. & Clarke, L.P. Review of MR image segmentation techniques using pattern recognition. Med. Phys. 20, 1033–1048 (1993).

    CAS  Google Scholar 

  16. Barbier, E.L. et al. Imaging cortical anatomy by high-resolution MR at 3.0T: detection of the stripe of Gennari in visual area 17. Magn. Reson. Med. 48, 735–738 (2002).

    Google Scholar 

  17. Fatterpekar, G.M. et al. Cytoarchitecture of the human cerebral cortex: MR microscopy of excised specimens at 9.4 Tesla. AJNR Am. J. Neuroradiol. 23, 1313–1321 (2002).

    Google Scholar 

  18. Pfeuffer, J., Merkle, H., Beyerlein, M., Steudel, T. & Logothetis, N.K. Anatomical and functional MR imaging in the macaque monkey using a vertical large-bore 7 Tesla setup. Magn. Reson. Imaging 22, 1343–1359 (2004).

    Google Scholar 

  19. Eickhoff, S. et al. High-resolution MRI reflects myeloarchitecture and cytoarchitecture of human cerebral cortex. Hum. Brain Mapp. 24, 206–215 (2005).

    Google Scholar 

  20. Koyama, M. et al. Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41, 795–807 (2004).

    CAS  Google Scholar 

  21. Uitti, R.J. et al. Magnetic resonance imaging and deep brain stimulation. Neurosurgery 6, 1423–1428 (2002).

    Google Scholar 

  22. Martin, A.J. et al. Placement of deep brain stimulator electrodes using real-time high-field interventional magnetic resonance imaging. Magn. Reson. Med. 54, 1107–1114 (2005).

    Google Scholar 

  23. Hall, W.A., Galichich, W., Bergman, T. & Truwit, C.L. 3-Tesla intraoperative MR imaging for neurosurgery. J. Neurooncol. 77, 297–303 (2006).

    Google Scholar 

  24. Susil, R.C. et al. Transrectal prostate biopsy and fiducial marker placement in a standard 1.5T magnetic resonance imaging scanner. J. Urol. 175, 113–120 (2006).

    Google Scholar 

  25. Logothetis, N., Merkle, H., Augath, M., Trinath, T. & Ugurbil, K. Ultra high-resolution fMRI in monkeys with implanted RF coils. Neuron 35, 227–242 (2002).

    CAS  Google Scholar 

  26. Lewis, J.W. & Van Essen, D.C. Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J. Comp. Neurol. 428, 79–111 (2000).

    CAS  Google Scholar 

  27. Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365 (2000).

    CAS  Google Scholar 

  28. Andersen, R.A., Mesallam, S. & Pesaran, B. Selecting the signals for a brain-machine interface. Curr. Opin. Neurobiol. 14, 720–726 (2004).

    CAS  Google Scholar 

  29. Schuirmann, D.J. A comparison of two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J. Pharmacokinet. Biopharm. 15, 657–680 (1987).

    CAS  Google Scholar 

  30. Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).

    Google Scholar 

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Acknowledgements

We thank T. Watanabe for technical assistance and M. Kinoshita for helpful comments on the development of the nonmagnetic mini-manipulator. This work was supported by a Grant-in-Aid for Specially Promoted Research from Ministry for Education, Culture, Sports, Science and Technology (MEXT) to Y.M (14002005), a Grant-in-Aid for Scientific Research from MEXT to K.N. (17500202) and Y.N. (15500206), and Japan Society for the Promotion of Science Research Fellowships for Young Scientists to K.W.K (1711962) and M.K. (1511804) and by Takeda Science Foundation.

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Correspondence to Yasushi Miyashita.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

A non-magnetic microdrive mini-manipulator for microelectrode implantation.

Supplementary Table 1

Scan parameters for magnetic resonance imaging of the phantom in vitro.

Supplementary Table 2

Scan parameters for magnetic resonance imaging of the monkeys in vivo.

Supplementary Table 3

Scan parameters for in vivo stability test of microelectrode position across days.

Supplementary Methods

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Matsui, T., Koyano, K., Koyama, M. et al. MRI-based localization of electrophysiological recording sites within the cerebral cortex at single-voxel accuracy. Nat Methods 4, 161–168 (2007). https://doi.org/10.1038/nmeth987

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