Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder
Major depressive disorder (MDD) is associated with complex disruptions in brain function, yet the underlying neural mechanisms remain incompletely understood. Traditional approaches to studying functional brain networks have primarily focused on pairwise interactions between brain regions, offering...
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IEEE
2024-01-01
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| Online Access: | https://ieeexplore.ieee.org/document/10811911/ |
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| author | Semen A. Kurkin Nikita M. Smirnov Rositsa Paunova Sevdalina Kandilarova Drozdstoy Stoyanov Larisa Mayorova Alexander E. Hramov |
| author_facet | Semen A. Kurkin Nikita M. Smirnov Rositsa Paunova Sevdalina Kandilarova Drozdstoy Stoyanov Larisa Mayorova Alexander E. Hramov |
| author_sort | Semen A. Kurkin |
| collection | DOAJ |
| description | Major depressive disorder (MDD) is associated with complex disruptions in brain function, yet the underlying neural mechanisms remain incompletely understood. Traditional approaches to studying functional brain networks have primarily focused on pairwise interactions between brain regions, offering valuable insights into basic connectivity. However, such methods often fail to capture the complexity of higher-order interactions that are critical for understanding integrative processes in the brain. This study aims to address this gap by applying Q-analysis, a mathematical framework that extends beyond pairwise interactions, to fMRI-derived brain networks to investigate higher-order interactions and structural organization in individuals with MDD compared to healthy controls (HCs). Our analysis revealed significant alterations in the topology of brain networks in MDD patients, characterized by a lower maximum topology level and an increased prevalence of isolated edges and chains at the pairwise interaction level. The substantia nigra area demonstrated a higher topological dimension in MDD, suggesting its greater integration into disrupted network structures, potentially reflecting dopaminergic dysfunction associated with the disorder. Additionally, the consensus networks at higher topology levels indicated distinct network configurations between MDD patients and HCs, with the former exhibiting a single q-connected component primarily involving limbic, cerebellar, and occipital-temporal regions. We identified significant disruptions in the higher-order organizational structures of the brain, characterized by reduced topological diversity and complexity, fewer and less connected cliques, and altered involvement of key brain regions in MDD: the increased engagement of the limbic structures such as the substantia nigra, parahippocampal gyrus, and hippocampus, and decreased involvement of the cerebellum, the occipital and temporal lobes. Our study introduces a novel approach to understanding MDD pathophysiology through the lens of higher-order network structures, offering potential avenues for more targeted diagnostic and therapeutic strategies. |
| format | Article |
| id | doaj-art-7cda036e4b794fdba6e5448b38fae0c9 |
| institution | Kabale University |
| issn | 2169-3536 |
| language | English |
| publishDate | 2024-01-01 |
| publisher | IEEE |
| record_format | Article |
| series | IEEE Access |
| spelling | doaj-art-7cda036e4b794fdba6e5448b38fae0c92024-12-31T00:00:47ZengIEEEIEEE Access2169-35362024-01-011219716819718610.1109/ACCESS.2024.352124910811911Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive DisorderSemen A. Kurkin0https://orcid.org/0000-0002-3438-5717Nikita M. Smirnov1https://orcid.org/0009-0002-7593-4345Rositsa Paunova2Sevdalina Kandilarova3Drozdstoy Stoyanov4https://orcid.org/0000-0002-9975-3680Larisa Mayorova5https://orcid.org/0000-0001-5112-7878Alexander E. Hramov6https://orcid.org/0000-0003-2787-2530Baltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University, Kaliningrad, RussiaBaltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University, Kaliningrad, RussiaDepartment of Psychiatry and Medical Psychology, Research Institute, Medical University of Plovdiv, Plovdiv, BulgariaDepartment of Psychiatry and Medical Psychology, Research Institute, Medical University of Plovdiv, Plovdiv, BulgariaDepartment of Psychiatry and Medical Psychology, Research Institute, Medical University of Plovdiv, Plovdiv, BulgariaFederal Research and Clinical Center of Intensive Care Medicine and Rehabilitology, Solnechnogorsk, RussiaBaltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University, Kaliningrad, RussiaMajor depressive disorder (MDD) is associated with complex disruptions in brain function, yet the underlying neural mechanisms remain incompletely understood. Traditional approaches to studying functional brain networks have primarily focused on pairwise interactions between brain regions, offering valuable insights into basic connectivity. However, such methods often fail to capture the complexity of higher-order interactions that are critical for understanding integrative processes in the brain. This study aims to address this gap by applying Q-analysis, a mathematical framework that extends beyond pairwise interactions, to fMRI-derived brain networks to investigate higher-order interactions and structural organization in individuals with MDD compared to healthy controls (HCs). Our analysis revealed significant alterations in the topology of brain networks in MDD patients, characterized by a lower maximum topology level and an increased prevalence of isolated edges and chains at the pairwise interaction level. The substantia nigra area demonstrated a higher topological dimension in MDD, suggesting its greater integration into disrupted network structures, potentially reflecting dopaminergic dysfunction associated with the disorder. Additionally, the consensus networks at higher topology levels indicated distinct network configurations between MDD patients and HCs, with the former exhibiting a single q-connected component primarily involving limbic, cerebellar, and occipital-temporal regions. We identified significant disruptions in the higher-order organizational structures of the brain, characterized by reduced topological diversity and complexity, fewer and less connected cliques, and altered involvement of key brain regions in MDD: the increased engagement of the limbic structures such as the substantia nigra, parahippocampal gyrus, and hippocampus, and decreased involvement of the cerebellum, the occipital and temporal lobes. Our study introduces a novel approach to understanding MDD pathophysiology through the lens of higher-order network structures, offering potential avenues for more targeted diagnostic and therapeutic strategies.https://ieeexplore.ieee.org/document/10811911/Higher-order interactionsfMRImajor depressive disorderfunctional brain networkQ-analysisclique |
| spellingShingle | Semen A. Kurkin Nikita M. Smirnov Rositsa Paunova Sevdalina Kandilarova Drozdstoy Stoyanov Larisa Mayorova Alexander E. Hramov Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder IEEE Access Higher-order interactions fMRI major depressive disorder functional brain network Q-analysis clique |
| title | Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder |
| title_full | Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder |
| title_fullStr | Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder |
| title_full_unstemmed | Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder |
| title_short | Beyond Pairwise Interactions: Higher-Order Q-Analysis of fMRI-Based Brain Functional Networks in Patients With Major Depressive Disorder |
| title_sort | beyond pairwise interactions higher order q analysis of fmri based brain functional networks in patients with major depressive disorder |
| topic | Higher-order interactions fMRI major depressive disorder functional brain network Q-analysis clique |
| url | https://ieeexplore.ieee.org/document/10811911/ |
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