Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Advances in Spinal Functional Magnetic Resonance Imaging in the Healthy and Injured Spinal Cords

Abstract

Purpose of Review

This review provides an overview of the current spinal functional magnetic resonance imaging (fMRI) studies that investigate the healthy and injured spinal cords.

Recent Findings

Spinal fMRI-derived outcome measures have previously been suggested to be sensitive to changes in neurological function in the spinal cord. A body of recent task-activated fMRI studies seems to confirm that detecting neural activity in the spinal cord using spinal fMRI may be feasible as well as reliable. Furthermore, a growing number of studies have shown that resting state fMRI in the spinal cord is also feasible, demonstrating that the investigation of changes in neural activity can also be performed in the absence of explicit tasks.

Summary

Current task-activated and resting state fMRI studies suggest that spinal fMRI has a strong potential to provide novel imaging biomarkers that can be used to investigate plastic changes in the injured spinal cord.

This is a preview of subscription content, log in to check access.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.

    Belegu V, Oudega M, Gary DS, McDonald JW. Restoring function after spinal cord injury: promoting spontaneous regeneration with stem cells and activity-based therapies. Neurosurg Clin N Am. 2007;18(1):143–68. xi.

  2. 2.

    McDonald JW, Sadowsky C. Spinal-cord injury. Lancet. 2002;359(9304):417–25.

  3. 3.

    Kirshblum S, Millis S, McKinley W, Tulsky D. Late neurologic recovery after traumatic spinal cord injury. Arch Phys Med Rehabil. 2004;85(11):1811–7.

  4. 4.

    Steeves JD, Lammertse D, Curt A, Fawcett JW, Tuszynski MH, Ditunno JF, et al. Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord. 2007;45(3):206–21.

  5. 5.

    Ellaway PH, Kuppuswamy A, Balasubramaniam AV, Maksimovic R, Gall A, Craggs MD, et al. Development of quantitative and sensitive assessments of physiological and functional outcome during recovery from spinal cord injury: a clinical initiative. Brain Res Bull. 2011;84(4–5):343–57.

  6. 6.

    Nebel MB, Joel SE, Muschelli J, Barber AD, Caffo BS, Pekar JJ, et al. Disruption of functional organization within the primary motor cortex in children with autism. Hum Brain Mapp. 2014;35(2):567–80.

  7. 7.

    Davey NJ, Nowicky AV, Zaman R. Somatopy of perceptual threshold to cutaneous electrical stimulation in man. Exp Physiol. 2001;86(1):127–30.

  8. 8.

    van Hedel HJ, Wirz M, Dietz V. Assessing walking ability in subjects with spinal cord injury: validity and reliability of 3 walking tests. Arch Phys Med Rehabil. 2005;86(2):190–6.

  9. 9.

    Catz A, Itzkovich M, Tesio L, Biering-Sorensen F, Weeks C, Laramee MT, et al. A multicenter international study on the Spinal Cord Independence Measure, version III: Rasch psychometric validation. Spinal Cord. 2007;45(4):275–91.

  10. 10.

    Stroman PW, Krause V, Malisza KL, Frankenstein UN, Tomanek B. Characterization of contrast changes in functional MRI of the human spinal cord at 1.5 T. Magn Reson Imaging. 2001;19(6):833–8.

  11. 11.

    • Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, et al. The current state-of-the-art of spinal cord imaging: methods. NeuroImage. 2014;84:1070–81. This paper provides one of the most comprehensive reviews of the spinal cord imaging, including spinal fMRI.

  12. 12.

    Choe AS, Belegu V, Yoshida S, Joel S, Sadowsky CL, Smith SA, et al. Extensive neurological recovery from a complete spinal cord injury: a case report and hypothesis on the role of cortical plasticity. Front Hum Neurosci. 2013 Jun 25;7:290.

  13. 13.

    Cadotte DW, Bosma R, Mikulis D, Nugaeva N, Smith K, Pokrupa R, et al. Plasticity of the injured human spinal cord: insights revealed by spinal cord functional MRI. PLoS One. 2012;7(9):e45560.

  14. 14.

    Stroman PW, Khan HS, Bosma RL, Cotoi AI, Leung R, Cadotte DW, et al. Changes in pain processing in the spinal cord and brainstem after spinal cord injury characterized by functional magnetic resonance imaging. J Neurotrauma. 2016;33(15):1450–60.

  15. 15.

    Zhong XP, Chen YX, Li ZY, Shen ZW, Kong KM, Wu RH. Cervical spinal functional magnetic resonance imaging of the spinal cord injured patient during electrical stimulation. Eur Spine J. 2017;26(1):71–7.

  16. 16.

    Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 1995;34(4):537–41.

  17. 17.

    Sherman JL, Nassaux PY, Citrin CM. Measurements of the normal cervical spinal cord on MR imaging. AJNR Am J Neuroradiol. 1990;11(2):369–72.

  18. 18.

    Sigmund EE, Suero GA, Hu C, McGorty K, Sodickson DK, Wiggins GC, et al. High-resolution human cervical spinal cord imaging at 7 T. NMR Biomed. 2011;25(7):891–9.

  19. 19.

    Kharbanda HS, Alsop DC, Anderson AW, Filardo G, Hackney DB. Effects of cord motion on diffusion imaging of the spinal cord. Magn Reson Med. 2006;56(2):334–9.

  20. 20.

    Verma T, Cohen-Adad J. Effect of respiration on the B0 field in the human spinal cord at 3T. Magn Reson Med. 2014;72(6):1629–36.

  21. 21.

    Topfer R, Starewicz P, Lo KM, Metzemaekers K, Jette D, Hetherington HP, et al. A 24-channel shim array for the human spinal cord: design, evaluation, and application. Magn Reson Med. 2016;76(5):1604–11.

  22. 22.

    Zhang B, Seifert AC, Kim JW, Borrello J, Xu J. 7 tesla 22-channel wrap-around coil array for cervical spinal cord and brainstem imaging. Magn Reson Med. 2016;17.

  23. 23.

    Ellingson BM, Sulaiman O, Kurpad SN. High-resolution in vivo diffusion tensor imaging of the injured cat spinal cord using self-navigated, interleaved, variable-density spiral acquisition (SNAILS-DTI). Magn Reson Imaging. 2010;28(9):1353–60.

  24. 24.

    Ben-Eliezer N, Sodickson DK, Shepherd T, Wiggins GC, Block KT. Accelerated and motion-robust in vivo T2 mapping from radially undersampled data using bloch-simulation-based iterative reconstruction. Magn Reson Med. 2016;75(3):1346–54.

  25. 25.

    Stroman PW, Ryner LN. Functional MRI of motor and sensory activation in the human spinal cord. Magn Reson Imaging. 2001;19(1):27–32.

  26. 26.

    Rossi C, Boss A, Steidle G, Martirosian P, Klose U, Capuani S, et al. Water diffusion anisotropy in white and gray matter of the human spinal cord. J Magn Reson Imaging. 2008;27(3):476–82.

  27. 27.

    Skare S, Andersson JL. On the effects of gating in diffusion imaging of the brain using single shot EPI. Magn Reson Imaging. 2001;19(8):1125–8.

  28. 28.

    Martin AR, Aleksanderek I, Cohen-Adad J, Tarmohamed Z, Tetreault L, Smith N, et al. Translating state-of-the-art spinal cord MRI techniques to clinical use: a systematic review of clinical studies utilizing DTI, MT, MWF, MRS, and fMRI. Neuroimage Clin. 2015;10:192–238.

  29. 29.

    Yoshizawa T, Nose T, Moore GJ, Sillerud LO. Functional magnetic resonance imaging of motor activation in the human cervical spinal cord. NeuroImage. 1996;4(3 Pt 1):174–82.

  30. 30.

    Stroman PW. Spinal fMRI investigation of human spinal cord function over a range of innocuous thermal sensory stimuli and study-related emotional influences. Magn Reson Imaging. 2009;27(10):1333–46.

  31. 31.

    Xie G, Piche M, Khoshnejad M, Perlbarg V, Chen JI, Hoge RD, et al. Reduction of physiological noise with independent component analysis improves the detection of nociceptive responses with fMRI of the human spinal cord. NeuroImage. 2012;63(1):245–52.

  32. 32.

    Kornelsen J, Smith SD, McIver TA, Sboto-Frankenstein U, Latta P, Tomanek B. Functional MRI of the thoracic spinal cord during vibration sensation. J Magn Reson Imaging. 2013;37(4):981–5.

  33. 33.

    Nash P, Wiley K, Brown J, Shinaman R, Ludlow D, Sawyer AM, et al. Functional magnetic resonance imaging identifies somatotopic organization of nociception in the human spinal cord. Pain. 2013;154(6):776–81.

  34. 34.

    Rempe T, Wolff S, Riedel C, Baron R, Stroman PW, Jansen O, et al. Spinal and supraspinal processing of thermal stimuli: an fMRI study. J Magn Reson Imaging. 2015;41(4):1046–55.

  35. 35.

    Light AR, Perl ER. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol. 1979;186(2):133–50.

  36. 36.

    Cohen AL, Fair DA, Dosenbach NU, Miezin FM, Dierker D, Van Essen DC, et al. Defining functional areas in individual human brains using resting functional connectivity MRI. NeuroImage. 2008;41(1):45–57.

  37. 37.

    Kelly C, Uddin LQ, Shehzad Z, Margulies DS, Castellanos FX, Milham MP, et al. Broca’s region: linking human brain functional connectivity data and non-human primate tracing anatomy studies. Eur J Neurosci. 2010;32(3):383–98.

  38. 38.

    Kim JH, Lee JM, Jo HJ, Kim SH, Lee JH, Kim ST, et al. Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: functional connectivity-based parcellation method. NeuroImage. 2010;49(3):2375–86.

  39. 39.

    Cramer SC, Lastra L, Lacourse MG, Cohen MJ. Brain motor system function after chronic, complete spinal cord injury. Brain. 2005;128(Pt 12):2941–50.

  40. 40.

    Winchester P, McColl R, Querry R, Foreman N, Mosby J, Tansey K, et al. Changes in supraspinal activation patterns following robotic locomotor therapy in motor-incomplete spinal cord injury. Neurorehabil Neural Repair. 2005;19(4):313–24.

  41. 41.

    Cramer SC, Orr EL, Cohen MJ, Lacourse MG. Effects of motor imagery training after chronic, complete spinal cord injury. Exp Brain Res. 2007 Feb;177(2):233–42.

  42. 42.

    • Barry RL, Smith SA, Dula AN, Gore JC. Resting state functional connectivity in the human spinal cord. elife. 2014;3:e02812. This is one of the first published studies of rsfMRI implemented within the spinal cord, which demonstrated that low-frequency BOLD fluctuations are inherent in the spinal cord as well as the brain.

  43. 43.

    • Kong Y, Eippert F, Beckmann CF, Andersson J, Finsterbusch J, Buchel C, et al. Intrinsically organized resting state networks in the human spinal cord. Proc Natl Acad Sci U S A. 2014;111(50):18067–72. This is one of the first published studies of spinal rsfMRI which identified spatially distinct RSNs in the human spinal cord using independent component analysis.

  44. 44.

    Vahdat S, Lungu O, Cohen-Adad J, Marchand-Pauvert V, Benali H, Doyon J. Simultaneous brain-cervical cord fMRI reveals intrinsic spinal cord plasticity during motor sequence learning. PLoS Biol. 2015;13(6):e1002186.

  45. 45.

    Liu X, Qian W, Jin R, Li X, Luk KD, Wu EX, et al. Amplitude of low frequency fluctuation (ALFF) in the cervical spinal cord with stenosis: a resting state fMRI study. PLoS One. 2016;11(12):e0167279.

  46. 46.

    Eippert F, Kong Y, Winkler AM, Andersson JL, Finsterbusch J, Buchel C, et al. Investigating resting-state functional connectivity in the cervical spinal cord at 3T. NeuroImage. 2017;147:589–601.

Download references

Acknowledgements

This work was supported in part by a grant from the Craig H. Neilsen Foundation (338419).

Author information

Correspondence to Ann S. Choe.

Ethics declarations

Conflict of Interest

Ann S. Choe declares no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by the author.

Additional information

This article is part of the Topical Collection on Spinal Cord Injury Rehabilitation

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Choe, A.S. Advances in Spinal Functional Magnetic Resonance Imaging in the Healthy and Injured Spinal Cords. Curr Phys Med Rehabil Rep 5, 143–150 (2017). https://doi.org/10.1007/s40141-017-0161-x

Download citation

Keywords

  • Spinal fMRI
  • Task-activated fMRI
  • Resting state fMRI
  • Spinal cord injury