Three dimensional echo-planar imaging at 7 Tesla

Abstract

Functional MRI (fMRI) most commonly employs 2D echo-planar imaging (EPI). The advantages for fMRI brought about by the increasingly popular ultra-high field strengths are best exploited in high-resolution acquisitions, but here 2D EPI becomes unpractical for several reasons, including the very long volume acquisitions times. In this study at 7 T, a 3D EPI sequence with full parallel and partial Fourier imaging capability along both phase encoding axes was implemented and used to evaluate the sensitivity of 3D and corresponding 2D EPI acquisitions at four different spatial resolutions ranging from small to typical voxel sizes (1.5–3.0 mm isotropic). Whole-brain resting state measurements (N = 4) revealed a better, or at least comparable sensitivity of the 3D method for gray and white matter. The larger vulnerability of 3D to physiological effects was outweighed by the much shorter volume TR, which moreover allows whole-brain coverage at high resolution within fully acceptable limits for event-related fMRI: TR was only 3.07 s for 1.5 mm, 1.88 s for 2.0 mm, 1.38 s for 2.5 mm and 1.07 s for 3.0 mm isotropic resolution. In order to investigate the ability to detect and spatially resolve BOLD activation in the visual cortex, functional 3D EPI experiments (N = 8) were performed at 1 mm isotropic resolution with parallel imaging acceleration of 3 × 3, resulting in a TR of only 3.2 s for whole-brain coverage.

From our results, and several other practical advantages of 3D over 2D EPI found in the present study, we conclude that 3D EPI provides a useful alternative for whole-brain fMRI at 7 T, not only when high-resolution data are required.

Introduction

Since the discovery of the BOLD effect, 2D gradient-echo echo-planar imaging (EPI) has been the workhorse of functional MRI, largely because of its high sampling speed and excellent sensitivity to signal changes related to brain activation, at both sufficient temporal (∼ 2–3 s) and spatial resolution (∼ 3–4 mm isotropic) with whole-brain coverage (Norris, 2006). Recently, it has been shown that higher spatial resolution would be beneficial to reduce the influence of physiological fluctuations (Triantafyllou et al., 2005, Triantafyllou et al., 2006). However, sampling at higher (isotropic) spatial resolution in conventional multi-slice 2D EPI considerably increases measurement times as the echo train length (ETL) becomes larger, and more slices have to be acquired to obtain the same covered volume. Methods such as partial Fourier (PF) sampling (Jesmanowicz et al., 1998) or partial parallel imaging (PPI) (Griswold et al., 2002, Pruessmann et al., 1999) provide an efficient means for shortening the ETL, and are hence well suited for obtaining high-resolution functional images, images with reduced EPI distortion artifacts (de Zwart et al., 2002, de Zwart et al., 2006, Preibisch et al., 2003, Schmidt et al., 2005), or single-shot acquisition of multiple echoes to improve BOLD sensitivity (Poser and Norris, 2009, Poser et al., 2006). Considerable effort has gone into the optimization of 2D EPI protocols and the practical challenges associated with fMRI at high field (Speck et al., 2008).

In the conventional 2D EPI sequence, slice selective excitation is performed and the signal subsequently acquired under an oscillating read and blipped phase encode gradient, so as to acquire the data for a full 2D image in a single shot within TR_slice. After repetition time TR_slice∙N_slices, all N_slices slices have been acquired, and the process is repeated. The effectiveness of both the PF and PPI methods for the reduction of acquisition time is hence rather limited in the case of 2D EPI, as the acceleration can only be performed along the (one and only) phase encode (PE) direction. The small potential time gain from under-sampling in 2D EPI is primarily due to the fact that TE should be kept constant to obtain the same functional contrast: For example, if the ETL is shortened by an acceleration factor of 2, the effective reduction in sampling time per slice is only TR_slice − ETL/4, which for a typical protocol is a time saving of only about 10%–15%.

Alternatively, a 3D sampling scheme can be employed whereby the same thick slab of tissue corresponding to the volume of interest is repeatedly excited, and a k_x–k_y plane of k-space acquired each time with a different k_z increment. For application to fMRI, this concept has attracted rapidly growing interest in the recent years, and 3D implementations with Cartesian (Poser and Norris, 2009, van der Zwaag et al., 2009) and spiral (Hu and Glover, 2007a, Hu and Glover, 2007b, Lai and Glover, 1998) k-space trajectory have been presented. For EPI-like sequences, a similar scheme was first suggested by Song et al. (1994) and Mansfield et al. (1995) who proposed to acquire even multiple k_z planes in a single shot. All these methods have in common that slice selection is replaced by a secondary phase encoding direction, and the complete 3D image then obtained by 3D Fourier transform upon acquisition of all k_z planes, again after time TR_slice∙N_slices. The important potential of 3D EPI here lies in the fact that entire k_z encoding steps (k_x–k_y planes) can be ‘skipped’ by the use of PF or PPI along the secondary phase direction, permitting considerable reductions in the volume sampling time TR_volume: For both these undersampling strategies, or their combination, the fractional time saving is directly given by the fraction of non-acquired secondary phase encodings. A 3D acquisition scheme where undersampling can be performed along the secondary PE direction will therefore be substantially more time efficient.

In terms of MR imaging, the implication of using 3D vs. 2D EPI is twofold. First, the time interval between subsequent excitations of the same tissue is much reduced, and as a result the steady state magnetization that is available for MR signal formation is lower; this is given by Eq. (1) and maximal when the flip angle α is equal to the Ernst angle (Eq. (2)) which should be calculated for the T₁ relaxation time of gray matter tissue. Second, the fact that N_slices more data points contribute to each data point in the 3D Fourier reconstruction leads to an intrinsic signal-to-noise (SNR) advantage of √N_slices which hence increases with increasing slice count.

$$M=M_0\sin \alpha \left(1-\exp \left(-\frac{\mathrm{T}{\mathrm{R}}_{slice}}{T_1}\right)\right)/\left(1-\cos \alpha \cdot \exp \left(-\frac{\mathrm{T}{\mathrm{R}}_{slice}}{T_1}\right)\right)$$

$${\alpha }_{\text{Ernst}}=\arccos \left(\exp \left(-\frac{\text{TR}}{T_1}\right)\right)$$

In this study, we propose the use of 3D EPI and to exploit the greater flexibility given by the second phase encoding along the third spatial dimension to either obtain higher spatial resolution within the same TR_volume, or to sample at the same spatial resolution within a much shorter time as compared to conventional 2D EPI. The proposed 3D EPI and conventional 2D EPI are compared by in vivo application with and without functional stimulation, and the various implications of using 3D EPI are discussed.