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Finger-Tapping Task fMRI in the Human Cervical Spinal Cord at 7T
Alan C Seifert1,2,3,4, Yazhuo Kong4,5, Karla L Miller4, Irene Tracey4, and S Johanna Vannesjo4

1Translational and Molecular Imaging Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United States, 2Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY, United States, 3Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, United States, 4Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom, 5Institute of Psychology, Chinese Academy of Sciences, Beijing, China

Synopsis

Functional MRI of the spinal cord is challenging due to its small size and deep anatomical location. Increasing field strength enhances BOLD signal and improves SNR, but B0 distortions produced by the lungs and vertebral column are amplified, presenting additional challenges in protocol optimization. Barry et al. have successfully performed resting-state fMRI at 7T; here, we present observations of robust, well-localized motor task activation in the human cervical spinal cord at 7T. We assessed single-shot and multi-shot EPI at two different resolutions. Multi-shot EPI achieved finer resolution and less spatial distortion in this preliminary 7T spinal cord task fMRI study.

Introduction

The spinal cord contains neural circuits that are scientifically and clinically of high interest [1], but fMRI of the spinal cord is challenging due to its small size and deep anatomical location [2]. Increasing field strength enhances BOLD signal and improves SNR, which yields finer spatial resolution, but also presents additional challenges: the lack of an RF body transmit coil necessitates specialized RF hardware [3,4], and magnetic field distortions produced by the lungs and vertebral column are amplified [5]. These factors make protocol development especially difficult, and little work has been done to explore optimal acquisition strategies. The lack of robust protocols has impeded progress in 7T spinal cord fMRI, which to date is limited to a few reports on resting-state fMRI [6]. In this study, we present preliminary observations of finger-tapping task activation in the human cervical spinal cord at 7T, and compare results obtained with single-shot and multi-shot EPI acquisitions at different resolutions.

Methods

Data were acquired in the cervical spinal cord (C4-C7 vertebral levels) of a healthy volunteer using a 7T whole-body MRI system (Magnetom, Siemens, Erlangen, Germany) and a volume-transmit, 16-channel receive cervical spine RF coil (Quality Electrodynamics, Mayfield Village, OH, USA). Three gradient-echo EPI protocols (single-shot 0.75mm resolution, and 4-shot 0.75mm/0.60mm resolution) were assessed; parameters are tabulated in Figure 1. Pulse-oximeter and respiratory traces were simultaneously acquired. Multi-shot reconstruction included a navigator-based per-shot frequency offset demodulation to mitigate respiratory field variations.

For each 6min 30s experiment, the subject performed 12 blocks of 20s rest and 10s task (tapping the thumb and first three fingers of the left hand at 3Hz), with a terminal 20s rest period. This task was expected to produce sensory activation in the ipsilateral dorsal horn at the neurological C6-C7 (vertebral C5-C6) level, and motor activation in the ipsilateral ventral horn at the neurological C7-C8 (vertebral C6-C7) level.

Four-dimensional image series were motion-corrected slicewise (x- and y-translation) using FSL FLIRT [7], and temporal SNR (tSNR) was calculated voxelwise as the temporal mean divided by temporal standard deviation. GLM analysis was performed within a mask of the spinal cord in FSL FEAT [8], incorporating a 37-term physiological noise model (8 cardiac, 8 respiratory, 16 interaction, heart rate, respiratory volume per time, CSF signal, and 2 motion correction terms) [9].

Results

Temporal mean images with overlaid activation maps for all three protocols are shown in Figure 2. Motor activity is observed in the ipsilateral ventral horn at vertebral level C6 in all three datasets (Fig. 2a,c,e, green arrows), while sensory activity is visible in the ipsilateral dorsal horn at vertebral level C5 in the single-shot dataset only (Fig. 2a, cyan arrow).

Plots of BOLD signal and model fits are shown in Figure 3 for the voxel with the greatest z-score within each dataset (Fig. 2a,c,e, green arrows). The highest z-score is observed in the single-shot 0.75mm dataset, while BOLD percent signal change (%SC) increases with effective image resolution (Fig. 4).

Focally high temporal SNR is observed in the center of the cord in the single-shot images (Fig. 2b), but tSNR averaged within the entire spinal cord is greatest in the 4-shot 0.75mm images (Fig. 4). The tSNR drops markedly towards lower slices in all three protocols (Fig. 5).

Discussion

The single-shot protocol has the highest steady-state NMR signal owing to the long TR, but is also more vulnerable to field inhomogeneities due to the long readout and TE. This leads to geometric distortion and signal loss, resulting in low tSNR especially at the periphery of the spinal cord and in lower slices. The effective resolution is also diminished by partial Fourier encoding and T2* blurring. Hence, relative to the single-shot image, the 4-shot images demonstrate greater resolution, greater BOLD %SC (perhaps due to reduced partial volume effect), markedly lower spatial distortion, and greater preservation of signal across the entire image volume.

While sensory activation is observed only in the single-shot image, this dataset also contains many false-positives; the activation patterns in the 4-shot datasets are highly specific to motor activity. These results, and resting-state fMRI results presented by Barry et al. [6], therefore support the advantages of multi-shot GRE methods for minimizing spatial distortion and maximizing resolution in 7T spinal cord fMRI. Multi-shot protocols are, however, more susceptible to time-varying fields, such as those caused by respiration, and rely on compensation for this effect both at the level of image reconstruction and time series analysis [5,6].

Conclusion

We have observed robust, well-localized motor task activation in the human cervical spinal cord at 7T using single-shot and multi-shot EPI.

Acknowledgements

This study was supported by National Institutes of Health (NINDS) award number K01NS105160 (ACS). This project has received funding from the Wellcome Trust (Strategic Award 102645/Z/13/Z, Senior Research Fellowship 202788/Z/16/Z) and from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 659263. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust (203139/Z/16/Z).

References

[1] Stroman PW, Wheeler-Kingshott C, Bacon M, et al. The current state-of-the-art of spinal cord imaging: methods. NeuroImage 2014;84:1070-1081.

[2] Cohen-Adad J. Functional Magnetic Resonance Imaging of the Spinal Cord: Current Status and Future Developments. Semin Ultrasound CT MRI 2017;38:176-186.

[3] 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. Magnetic Resonance in Medicine 2017;78(4):1623-1634.

[4] Barry RL, Vannesjo SJ, By S, Gore JC, Smith SA. Spinal Cord MRI at 7T. NeuroImage 2018;168:437-451.

[5] Vannesjo SJ, Miller KL, Clare S, Tracey I. Spatiotemporal characterization of breathing-induced B0 field fluctuations in the cervical spinal cord at 7T. NeuroImage 2018;167:191-202.

[6] Barry RL, Smith SA, Dula AN, Gore JC. Resting state functional connectivity in the human spinal cord. Elife 2014;3:02812.

[7] Jenkinson M, Smith SM. A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2):143-156, 2001.

[8] Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data. NeuroImage 2001;14(6):1370-1386.

[9] Kong Y, Jenkinson M, Andersson JLR, Tracey I, Brooks JCW. Assessment of physiological noise modelling methods for functional imaging of the spinal cord. NeuroImage 2012;60(2):1538-1549.

Figures

Figure 1: Acquisition parameters for the single-shot and two multi-shot gradient-echo EPI protocols compared in this study (a). The Ernst angle was not achieved in any protocol; instead, TR was optimized, and the flip angle was constrained by SAR limits. The position of the slice packet covering vertebral levels C4-C7 (yellow) and the volume for shim optimization (green) are also shown (b-d).

Figure 2: Temporal mean images with overlaid activation maps (a,c,e) and temporal SNR maps (b,d,f) for all three protocols. Motor activity in the ipsilateral ventral horn at vertebral level C6 is indicated by green arrows in all three datasets (a,c,e). Sensory activity, indicated by a cyan arrow, is visible in the ipsilateral dorsal horn at vertebral level C5 in the single-shot dataset (a). Focally high temporal SNR is observed in the center of the cord in the single-shot images (b), but temporal SNR averaged in a mask of the entire spinal cord is greatest in the 4-shot 0.75mm images (d).

Figure 3: Plots of BOLD signal and model fits, averaged by stimulus block, for the voxel with the highest z-score in the area of expected motor activation within each dataset. These voxels are indicated by green arrows in Figure 2a,c,e.

Figure 4: Temporal SNR averaged within a mask of the entire spinal cord, and BOLD percent signal change and z-statistic observed in the most significantly activated voxel in the area of expected motor activation within each dataset. These voxels are indicated by green arrows in Figure 2a,c,e.

Figure 5: Temporal SNR in each image slice, averaged within a mask of the spinal cord. Lower slice numbers correspond to more inferior slices. The most inferior slices, at the C7 vertebral level, are most strongly affected by field distortions due to respiration, and are outside the most efficient and sensitive regions of the RF coil’s transmit and receive B1 fields. These effects contribute to significantly reduced temporal SNR compared to more superior slices.

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
0298