Sjir Schielen1, Dmitrii Stepanov1, Ramona Cîrstian2, Albert Aldenkamp1,3, and Svitlana Zinger1,3
1Electrical Engineering, Eindhoven University of Technology, Eindhoven, Netherlands, 2Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands, 3Epilepsy Center Kempenhaeghe, Heeze, Netherlands
Synopsis
Keywords: Psychiatric Disorders, fMRI (resting state), Neuropsychiatric disorders, effective connectivity, neurodynamics
Motivation: The diagnosis of major depressive disorder (MDD) currently involves subjectivity, but an objective test based on a measurement is desired.
Goal(s): To obtain effective connections between brain networks from functional MRI that both allow MDD to be diagnosed and offer clinically relevant insight.
Approach: Stochastic Dynamic Causal Modelling is applied to the time series of resting-state networks. The most discriminative connections are found through Bayesian Model Reduction and Chi-Square feature selection. These connections are used for classification using machine learning.
Results: Eight clinically relevant effective connections result in 94% leave-one-out cross-validation accuracy, which resulted in 100% accuracy on a separate test set.
Impact: The discriminative ability of the eight resulting effective connections aid understanding of MDD's pathophysiology. Furthermore, the results may inspire researchers to investigate the eight most discriminative connections on other datasets, which can lead to an objective diagnostic biomarker for MDD.
Introduction
While an objective diagnosis of major
depressive disorder (MDD) progressing from a measurement is desired1,
the diagnosis is still based on criteria prone to subjectivity2. Functional
magnetic resonance imaging (fMRI) provides measurements of the brain over time,
which allows the blood-oxygen-level-dependent (BOLD) signal to be extracted.
The BOLD signal serves as a proxy of neuronal activity, which has been analyzed
for diagnostic purposes and biomarker discovery3. Where most studies
look at functional connectivity between regions of interest (ROIs)4,
we think effective connectivity (EC), i.e. causal relations rather than
correlations, allows a deeper understanding of MDD’s underlying
pathophysiology. While data-driven methods to extract causal relations like Granger
causality5, 6 are more commonly used for EC, we leveraged Friston’s biologically-inspired
method titled stochastic Dynamic Causal Modelling 7, 8 (sDCM) as it
is tailored to neuronal activity. Though some studies have applied DCM to MDD4, 9, 10, this is, to our knowledge, the first study that applies sDCM on resting-state
networks (RSNs) to obtain effective connections capable of diagnosing MDD. The
most discriminative connections relate to MDD’s symptoms, which may show merit
in the discovery of a biomarker. This is also important in the light of trauma, as depression is the most common neuropsychiatric disorder following traumatic brain injury11. Methods
BOLD time series are adopted6, which represent the activity of each RSN (Fig. 1) in time per individual. Effective
connections (matrix $$$A$$$) are
estimated following sDCM’s neuronal-inspired model (Fig. 2). A hemodynamic model
is used to generate a signal from $$$A$$$ based on assumed biophysical influences and
noise. The generated signal is then assessed on what percentage of the variance
of the observed BOLD signal it explains. The group-average effective
connections $$$A_{MDD}$$$ and $$$A_{control}$$$ are obtained from each individual’s $$$A$$$ using Parametric Empirical Bayes12.
Bayesian Model Reduction9 is used to eliminate non-contributing connections.
The contributing effective connections are further reduced using Chi-Square
feature selection. Multiple classifiers (SVM, KNN, Trees) are trained and
validated using leave-one-out cross-validation (LOOCV) on 70% of the dataset. The
trained and validated models are tested on the 30% hold-out data. The selected
features are discussed with a neurologist for clinical interpretation. Results
Analyses were performed using DCM12.5 in
SPM12 for Matlab R2023a. The open-source dataset13 comprises 51
individuals with MDD and 21 healthy controls. Demographic and clinical data are
listed in Table 1. The fitted sDCM models explained between 75% and 90% of the variance in the participant's BOLD signals, making them good models. Bayesian Model Reduction and Chi-Square
feature selection resulted in eight effective connections that were
consistently the most discriminative between the groups. These connections are shown in Fig. 3 and their weights are used
for classification. The results of LOOCV and performance
on the separate test set are listed in Table 2. A linear support vector machine
performed best in LOOCV and obtained 100% accuracy on the test set. Discussion
While the results of the methodology are
promising, they are obtained on a dataset that does not incorporate cross-site
heterogeneity. MDD is a heterogeneous disorder and different MRI scan protocols
may add further heterogeneity. Therefore, future work should investigate if (a
subset of) the same effective connections (Fig. 3) can reproduce the
discriminative ability shown in this study. What could indicate that
these connections are in the right direction is clinical interpretation. Depressed
people tend to lack initiation which can be linked to a lower excitatory
connection between the default mode network and the executive network. Furthermore,
inhibitory connections from and to the dorsal attention network can be linked to
distractibility and a loss of pleasure in normal activities. The connection
between the sensorimotor network and the dorsal attention network is not surprising
as both relate to information processing. The cause and effect of MDD cannot be
disentangled from these results, but the differences in connections are in line
with part of the observations and symptoms of MDD2.Conclusion
The identified effective connections show
clinical interpretability and the capability to discriminate between individuals with major depressive disorder and healthy controls. If the same effective connections can be reproduced on other
datasets, this is a major stride toward an objective biomarker for major
depressive disorder.Acknowledgements
No acknowledgement found.References
- Insel T, Cuthbert B, Garvey M, et al. Research
domain criteria (RDoC): toward a new classification framework for research on
mental disorders. American
Journal of Psychiatry. 2010;167(7):748-751.
- American Psychiatric Association.
Diagnostic and statistical manual of mental disorders: DSM-5. American
Psychiatric Publishing; 2013.
- Wang L, Hermens DF, Hickie IB, et al. A systematic review of resting-state functional-MRI
studies in major depression. Journal of Affective Disorders. 2012;142(1-3):6-12.
- Pilmeyer J, Huijbers W, Lamerichs R, et al. Functional
MRI in major depressive disorder: A review of findings, limitations, and future
prospects. Journal of Neuroimaging. 2022;32(4):582-595.
- Yang C, Xiao K, Ao Y, et al. The
thalamus is the causal hub of intervention in patients with major depressive
disorder: Evidence from the Granger causality analysis. NeuroImage: Clinical. 2022;103295.
- Cîrstian R, Pilmeyer J, Bernas A, et al. Objective biomarkers of depression: A study of
Granger causality and wavelet coherence in resting‐state fMRI. Journal of Neuroimaging. 2023;33(3):404-414.
- Friston KJ, Harrison L, Penny W. Dynamic causal modelling. Neuroimage. 2003;19(4):1273-1302.
- Friston KJ, Kahan J, Biswal B, et al. A dcm for resting state fmri. Neuroimage. 2014;94:396-407.
- Li G, Liu Y, Zheng Y, et al. Large‐scale dynamic causal
modeling of major depressive disorder based on resting‐state functional magnetic
resonance imaging. Human Brain Mapping. 2020;41(4):865-881.
- Geng X, Xu J,
Liu B, et al. Multivariate classification of major depressive
disorder using the effective connectivity and functional connectivity. Frontiers in Neuroscience. 2018;12:38.
- Albrecht JS, Barbour L, Abariga S, et al. Risk of depression after traumatic brain
injury in a large national sample. Journal of Neurotrauma. 2019;36(2):300-307.
- Zeidman P, Jafarian A, Seghier M, et al. A guide to
group effective connectivity analysis, part 2: Second level analysis with PEB. Neuroimage. 2019;200:12-25.
- Bezmaternykh DD,
Melnikov ME, Savelov AA, et al. Resting state with closed eyes for patients with depression and
healthy participants. OpenNeuro. April 2020. https://openneuro.org/datasets/ds002748/versions/1.0.0. Accessed December 13, 2022.