Rebecca Susan Dewey1,2,3, Deborah A Hall2,3,4, Christopher J Plack5,6,7, and Susan T Francis1
1Sir Peter Mansfield Imaging Centre, School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom, 2NIHR Nottingham Biomedical Research Centre, Nottingham, United Kingdom, 3Hearing Sciences, Division of Clinical Neuroscience, School of Medicine, University of Nottingham, Nottingham, United Kingdom, 4University of Nottingham Malaysia, Jalan Broga, Selangor Darul Ehsan, Malaysia, 5Manchester Centre for Audiology and Deafness (ManCAD), University of Manchester, Manchester, United Kingdom, 6NIHR Manchester Biomedical Research Centre, Manchester, United Kingdom, 7Department of Psychology, Lancaster University, Lancaster, United Kingdom
Synopsis
We compared cortical and subcortical auditory BOLD fMRI
responses to epochs of broadband noise acquired using continuous sampling with active
noise cancellation (TR = 2s) to sparse sampling (TR = 8s, 1993ms acquisition with
6007ms silence) in a repeated measures factorial design. High resolution (1.5
mm3) 3 Tesla fMRI data were acquired using multiband 2 and corrected
for physiological noise and image distortions. BOLD beta estimates are compared
for onset, offset and sustained auditory fMRI responses for both sampling schemes.
We report the strengths and weaknesses of the two sampling methods.
Introduction
fMRI of the auditory pathway requires perception of a
salient auditory stimulus compared to a “silent” baseline period. It has been
shown that “higher” sections of the pathway (upper-midbrain/cortex) respond
preferentially to transient stimuli whilst “lower” regions (brainstem) respond more
to sustained acoustic energy [1]. However, the baseline period of auditory fMRI
is confounded by acoustic noise from imaging gradients. Two approaches to reduce
the impact of scanner acoustic noise are (i) “sparse” temporal sampling of single
brain volumes, providing intervals with no scanner acoustic noise [2]; or (ii) active
noise cancellation, with commercially-available systems generating acoustic
signals that add destructively with the scanner acoustic noise to significantly
reduce the overall acoustic energy at the eardrum of the participant [3]. Here,
we use a broadband noise block design for optimal activation of subcortical regions,
comparing these two sampling approaches to assess sustained and transient
auditory responses in subcortical and cortical auditory regions.Methods
15 participants (n=11 female; age=33±11 years) with self-reported
normal hearing were scanned on a Philips Ingenia 3.0 T MR scanner with 32-channel
head coil using a gradient-echo EPI readout (TE=34ms, FOV=168×168mm, 1.5mm isotropic resolution, SENSE2,
multiband2, halfscan=0.927). 46 coronal-oblique slices provide coverage of the
brainstem and Heschl’s gyrus. Continuous sampling was performed with a TR=2s and equidistant
temporal slice spacing, sparse sampling had a 1993ms image acquisition (TA) followed
by 6007ms silence (effective TR=8s).
Each fMRI run comprised 12 cycles of 24-s broadband
noise (1.4-4.1 kHz; 85 dB-SPL) and 24-s rest resulting in 144/36 acquisitions for
noise and rest for continuous/sparse sampling. Stimuli were presented using the
OptoACTIVE Optical MRI Communication System (Optoacoustics Ltd., Israel) with active
noise cancellation (reducing scanner acoustic noise to 70 dB-SPL) during continuous sampling
only. Both acquisitions were synchronous with the start of the stimulus.
Two continuous and two sparse sampling fMRI runs were collected per individual
in a randomised order. Additionally, EPI dynamics with (i) echo shift and (ii) reversed
phase-encoding gradient were collected for distortion correction, and also MPRAGE structural
images.
fMRI data were motion corrected, distortion corrected
using FSL TOPUP [4,5], RETROICOR physiological noise corrected [6], spatially
smoothed (2mm) and analysed in SPM12. Statistical analyses were performed using
a GLM of responses to onset and offset, modelled as a stimulus duration=0 at
the start/end of broadband noise, and the sustained stimulus, including motion
parameters, white matter and CSF as nuisance regressors. A random-effects group
analysis was performed to generate SPMs for onsets, offsets and sustained
responses using both sampling methods. Region of interest (ROI) masks were
formed by thresholding (p<0.001 uncorrected; k=5) SPMs to sustained
responses/onsets/offsets for both sampling schemes. Masks were combined (“OR”)
to form a single binary mask defining statistically significant sound-related
activity which was divided into brainstem, midbrain and cortical ROIs (Figure 1).
We evaluate the impact of continuous or sparse sampling on the mean ROI fMRI beta
estimates.
Results
Figure 2 shows group activation maps of the auditory
pathway and Figure 3 the timecourse from continuous sampling. Stronger cortical
responses to the stimulus onset are seen for continuous sampling. Stronger subcortical
responses to the sustained stimulus using sparse sampling. Figure 4 shows the fMRI
beta estimates in brainstem, midbrain and cortical ROIs for both sampling schemes.
ANOVA statistics showed a significant effect of sampling scheme (F=29.192;
d.f.=1,14; p<0.001) and ROI (F=15.755; d.f.=2,28; p<0.001), and
significant interactions for ROI*sampling scheme (F=20.348; d.f.=2,28; p<0.001)
and ROI*stimulus (F=12.120; d.f.=4,56; p<0.001), demonstrating that the two
schemes were selectively preferable for different ROIs of the auditory pathway.
As expected, image signal-to-noise ratio (SNR) was higher for sparse than
continuous sampling [cortex: 106±12/85±8, brainstem: 111±12/86±8 for
sparse/continuous], along with temporal SNR [cortex: 29±1/23±1, brainstem: 14±1/11±1
for sparse/continuous].Discussion
The higher temporal sampling of continuous is
superior to sparse sampling for detection of the transient (onset/offset)
responses dominant in the auditory cortex. In contrast, sparse sampling was
superior to continuous sampling with active noise cancellation in detecting the
sustained responses in the subcortical regions. Gains may be explained in terms
of reduced interference by scanner acoustic noise and increased SNR from full T1
recovery between acquisitions. It is important to note that a continuous
broadband stimulus was selected to stimulate brainstem rather than cortex alone.
Future studies will assess the impact of alternative sparse or clustered acquisition
timings on functional contrast to maximize both cortical and brainstem
responses for sparse sampling.Conclusion
An optimised multiband-sparse fMRI protocol provides
significant improvements over multiband-continuous acquisitions to study
sustained auditory responses in subcortical regions, even when active noise
cancellation is used.Acknowledgements
This work is supported by Medical Research Council
(MRC) reference MR/L003589/1 awarded to the University of Manchester.References
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