Sonja Blankenagel1,2, Ana Beatriz Solana3, Brice Fernandez4, Christoph Hofstetter5, Andreas Dunkel5, Thomas Hofmann5, Hans Hauner6,7, and Jessica Freiherr1,2
1Fraunhofer Institute for Process Engineering and Packaging (IVV), Freising, Germany, 2Diagnostic and Interventional Neuroradiology, RWTH Aachen University, Aachen, Germany, 3GE Global Research, Munich, Germany, 4GE Healthcare, Orsay, France, 5Food Chemistry and Molecular Sensory Science, Technical University of Munich, Freising, Germany, 6ZIEL Institute for Food and Health, Clinical Nutritional Medicine, Technical University of Munich, Munich, Germany, 7Institute of Nutritional Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
Synopsis
Multi‑echo planar
imaging (MEPI) was explored regarding its ability to overcome the limitations
of conventional EPI imaging in studies related to olfaction. MEPI offers great
sensibility even in brain regions, which are affected by susceptibility
artifacts in EPI imaging. Five subjects were scanned using an event-related
olfactory task with both sequences. The subsequent comparison shows that three
echoes MEPI has advantages regarding olfaction-related brain activation
compared to single echo EPI.
Introduction
The measurement of
brain activation during sensory perception using functional magnetic resonance
imaging (fMRI) is limited by magnetic field inhomogeneity in the brain areas
adjacent to the nose and ears. This makes it difficult to show the primary
processing steps in olfaction [1].
We, therefore, explored
images acquired with a novel sequence, namely multi‑echo echo planar imaging
(MEPI) for its ability to overcome the limitations of brain imaging by
conventional echo-planar imaging (EPI). The combination of three echo times in
MEPI can compensate signal and BOLD sensitivity losses in EPI [2–5]
Methods
Five healthy volunteers
(all females) participated in our scanning session with the two different
sequences. We used olfactory stimulation with two food-related odors, one
attractive and one aversive, as a model approach to compare the three sequences
and identify their strengths and weaknesses in the context of imaging olfactory
processing. Odors were delivered using a constant-airflow olfactometer [6] during 3 seconds after an auditory sniff cue to the subjects. In the
control condition the headspace of water was delivered by the olfactometer,
presenting no odor to the participant. As an attractive, food-related odor we
used strawberry [7], and as an aversive, food-related odor we used liver [8].
This event-related
olfactory fMRI task was conducted in a GE Discovery MR750w 3T scanner with a
12-channel head coil. Two pulse sequences were used for each volunteer in a
randomized order: A standard EPI and a three echoes MEPI [4]. The main sequence
parameters for both sequences were, respectively: TR = 2 s / 2.5 s, TEs = 30 / 14.4,
35.5, 56.5 ms, FA = 77° / 83º, matrix = 80 x 80 / 64 x 50, FoV = 20.0 cm, slice
thickness = 2.5 mm, gap = 0.5 mm, # slices = 32 / 22, ASSET = 2.
Analysis of the fMRI
data was conducted using SPM12 based on Matlab except for the slice time
correction and realignment steps for MEPI followed by the combination of the
images of different TEs (echo times), which were conducted in SPM8 [4,5]. Fixed-effects group analysis was conducted with five subjects per
sequence for the condition odor versus non-odor.Results
Using MEPI, activation
of typical olfactory brain regions (piriform cortex) was established even with
a low subject number and at a lower significance level than conventional EPI.
At a significance level of p < 0.001 (uncorrected for whole-brain comparison),
MEPI data of five subjects show activation of the piriform cortex while in EPI
no suprathreshold clusters survived (Figure 1). For visualization purposes a
lower threshold of p < 0.01 uncorrected was used. Here, activation of the
piriform cortex can be shown by EPI only on the left hemisphere, while using MEPI
we find stronger activation not only in bilateral piriform cortex but also
bilaterally in the orbitofrontal cortex (Figure 2).Discussion
We conclude that MEPI
is well suited for sensory stimulation scenarios including olfaction. This
sequence is more potent to show olfaction-related brain activations than EPI,
even at low number of subjects. On the other hand, MEPI cannot achieve the same
brain coverage and spatial resolution as the conventional EPI even for longer TR
(repetition time) (Figure 3). However, shorter readouts for MEPI could be
achieved by the use of partial Fourier or higher acceleration factors for
32-channel head coil. Also, the next step could include the use of multiband
(multislice) MEPI, which will allow an increase of the number of slices in the
same amount of time [9].
In conclusion, we were
able to establish an improvement in the visualization of olfaction-related
brain activation using MEPI instead of EPI. Further optimization work should
target the improvement of brain coverage to make MEPI a useful tool also in
studies targeting multisensory integration processes.Acknowledgements
We thank Prof. Dr.
Haase (IMETUM, TU Munich) and Dr. Schirmer (GE Global Research, Garching) for
collaboration at the MRI machine and our volunteers for participation.References
[1] C. Moessnang, J. Freiherr,
Olfaktorik, in: F. Schneider (Ed.), Funktionelle MRT in Psychiatrie und
Neurologie, 2nd ed., Springer, Berlin, 2013. ISBN: 978-3-642-29800-4,
pp. 505–521.
[2] P. Kundu, S.J. Inati, J.W.
Evans, W.-M. Luh, P.A. Bandettini, Differentiating BOLD and non-BOLD signals in
fMRI time series using multi-echo EPI, NeuroImage 60 (3) (2012) 1759–1770. DOI:
10.1016/j.neuroimage.2011.12.028.
[3] O. Speck, J. Hennig, O. Speck,
J. Hennig, Functional imaging by I0- and T2*-parameter mapping using
multi-image EPI, Magnetic resonance in medicine 40 (2) (1998) 243–248. DOI:
10.1002/mrm.1910400210.
[4] B. Fernandez, L. Leuchs, P.
Sämann, M. Czisch, V. Spoormaker, Application of multi-echo EPI on a fear
conditioning task: evidence of improved BOLD detection in ventromedial
prefrontal cortex: 29 (Suppl 1):S247–S400 (338), Vienna, Austria, 2016.
[5] B.A. Poser, M.J. Versluis, J.M.
Hoogduin, D.G. Norris, BOLD contrast sensitivity enhancement and artifact
reduction with multiecho EPI: parallel-acquired inhomogeneity-desensitized
fMRI, Magnetic resonance in medicine 55 (6) (2006) 1227–1235. DOI:
10.1002/mrm.20900.
[6] J.N. Lundström, A.R. Gordon,
E.C. Alden, S. Boesveldt, J. Albrecht, Methods for building an inexpensive
computer-controlled olfactometer for temporally-precise experiments,
International journal of psychophysiology official journal of the International
Organization of Psychophysiology 78 (2) (2010) 179–189. DOI:
10.1016/j.ijpsycho.2010.07.007.
[7] P. Schieberle, T. Hofmann,
Evaluation of the Character Impact Odorants in Fresh Strawberry Juice by
Quantitative Measurements and Sensory Studies on Model Mixtures, J. Agric. Food
Chem. 45 (1) (1997) 227–232. DOI: 10.1021/jf960366o.
[8] S. Straßer, Characterisation of
the key aroma compounds in processed duck liver: Studies on their formation
during roasting and differences to livers of other animal species, 1st ed.,
Verl. Deutsche Forschungsanst. für Lebensmittelchemie (DFA), Freising, 2012.
ISBN: 978-3-938896-52-5.
[9] V. Olafsson, P. Kundu, E.C.
Wong, P.A. Bandettini, T.T. Liu, Enhanced identification of BOLD-like
components with multi-echo simultaneous multi-slice (MESMS) fMRI and multi-echo
ICA, NeuroImage 112 (2015) 43–51. DOI: 10.1016/j.neuroimage.2015.02.052.