Karthik R Sreenivasan1, Xiaowei Zhuang1, Virendra Mishra1, Zhengshi Yang1, Gopikrishna Deshpande2, Sarah Banks1, and Dietmar Cordes1
1Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, United States, 2AU MRI Research Center, Department of Electrical and Computer Engineering, Auburn University, Auburn, AL, United States
Synopsis
Current study used fMRI to investigate
differences in effective connectivity and network topology between a group of
trained master sommeliers and untrained control participants during olfactory
tasks. Master sommeliers showed stronger connectivity originating
from regions involved in higher-level cognitive processes than the controls.
There was also increased small-world topology in the sommeliers. These findings
provide unique insights into the neuroplasticity in adulthood in the olfactory
network which may have added clinical importance in diseases like Alzheimer’s
and Parkinson’s where early neurodegeneration is isolated to regions important
in smell.Introduction
Previous studies investigating the
differences in olfactory processing and judgments between trained sommeliers
and control participants have shown increased activations in brain regions
involving higher-level cognitive processes in sommeliers [1, 2]. Despite these
findings, there is little or no information about the influence of expertise on
causal connectivity and topological properties of the connectivity networks
between these regions. Therefore, the current study focuses on addressing these
questions in an fMRI study of olfactory perception in trained master sommeliers.
Method
FMRI data were acquired from thirteen master
sommeliers and thirteen control participants during different olfactory and
non-olfactory tasks. A single odorant was presented during the olfactory tasks and
the participants were informed as to which olfactory task to perform. For one
of the olfactory tasks, participants reported whether odorant was wine or
non-wine, and for the other they reported if the odorant presented was red or
white wine. One of the non-olfactory task was a visual discrimination task
during which participants were randomly presented a pixelated image of a
fingerprint or zebra skin and asked to identify the image correctly. The other
non-olfactory task was a motor task, where the participants were delivered a
stream of air without any odorant and asked to respond with a button press. After
standard pre-processing using SPM12, mean time series were extracted from 76
different ROIs (based on AAL [3] and Jülich atlas [4]) and underlying neuronal
variables were extracted using Cubature Kalman filter based blind hemodynamic
deconvolution [5]. The resultant neuronal variables were then input into a
dynamic multivariate autoregressive [6, 7] model to obtain connectivity between
every pair of ROIs as a function of time. The absolute causal connectivity
values during task of interest (for wine/non wine task and fingerprint or zebra
task) were then populated into different samples separately for the sommelier
and control groups. One-sided two-sample t-tests were performed between these
samples and paths that were significantly greater during the wine/non-wine task
were identified. Among these, paths that were significantly different between
the sommeliers and controls were obtained. The obtained connectivity matrices
were further studied using graph theory by labeling effective connectivity (EC)
as an edge and a brain region as a node. Using Brain Connectivity Toolbox [8]
the small-world parameters were obtained at different sparsity thresholds (0.1
< S < 0.98, ∆S = 0.01) for each participant and compared between the two
groups.
Results
There were a total of 80 EC paths that were
significantly different (p<0.01 nonparametric testing [9]) between the two
groups (54 paths were significantly greater in sommeliers compared to controls
and 26 paths were significantly greater in controls compared to sommeliers).
For simplicity, fig. 1 shows only those EC paths that were extremely
significant (p<<0.01, t-value > 9) in the between-group comparison. It
can be seen that there are two different connectivity networks that exist in
the two groups. The right paracentral lobule (PCL) is a major hub in the
controls, while the left thalamus (THA) and the left inferior occipital gyrus
(IOG) are hubs in the sommeliers. Fig. 2 shows the differences in overall
network characteristics between the two groups. The connectivity networks of
both the groups represented a small-world organization for a defined range of sparsity.
Subsequent evaluation of the integrated area under the curve (AUC) values over
the range of sparsity showed significantly higher small-world index, normalized
clustering coefficient and normalized path length in master sommeliers when
compared to untrained participants (p<0.05 corrected, effect size > 1).
Conclusion
The current study revealed differences in causal
connectivity and topological properties of networks involved in olfactory
perception among master sommeliers and untrained control participants. Specifically
connections from the left THA and the left IOG were significantly greater in
sommeliers and connections from right PCL were greater in controls.
Furthermore, both groups showed a small-world organization, but the master
sommeliers exhibited significantly increased small-world topology as compared
to the controls. These observations support the view that specialized expertise
and training might result in enhancements in the brain well into adulthood. These
findings are mainly important, given the fact that, learning about
neuroplasticity in adulthood in these regions may, then, have added clinical
importance in diseases like Alzheimer’s and Parkinson’s where early
neurodegeneration is isolated to regions important in smell.
Acknowledgements
This study was funded via the Director’s Innovation Fund, we thank Dr.
Jeffrey Cummings for making the funds available.References
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