Diffusion time-related structure-function coupling reveals differential association with inter-individual variations in body mass index

•Structure-function coupling related to body mass index (BMI) was investigated.•We simulated functional connectivity from structural data using Riemannian approach.•BMI-related alterations in coupling were most clear when the hierarchy was evident.•Alterations were most obvious in the transmodal reg...

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Veröffentlicht in:NeuroImage (Orlando, Fla.) Jg. 291; S. 120590
Hauptverfasser: Namgung, Jong Young, Park, Yeongjun, Park, Yunseo, Kim, Chae Yeon, Park, Bo-yong
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Elsevier Inc 01.05.2024
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ISSN:1053-8119, 1095-9572, 1095-9572
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Abstract •Structure-function coupling related to body mass index (BMI) was investigated.•We simulated functional connectivity from structural data using Riemannian approach.•BMI-related alterations in coupling were most clear when the hierarchy was evident.•Alterations were most obvious in the transmodal regions.•Cytoarchitecture and transcriptomic analyses provided biological underpinnings. Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with altered brain structure and function. However, the mechanism underlying the alteration of structure-function correspondence according to BMI is under-investigated. In this study, we studied structural and functional connectivity derived from diffusion MRI tractography and inter-regional correlations of functional MRI time series, respectively. We combined the structural and functional connectivity information using the Riemannian optimization approach. First, the low-dimensional principal eigenvectors (i.e., gradients) of the structural connectivity were generated by applying diffusion map embedding with varying diffusion times. A transformation was identified so that the structural and functional embeddings share the same coordinate system, and subsequently, the functional connectivity matrix was simulated. Then, we generated gradients from the simulated functional connectivity matrix. We found the most apparent cortical hierarchical organization differentiating between low-level sensory and higher-order transmodal regions in the middle of the diffusion time, indicating that the hierarchical organization of the brain may reflect the intermediate mechanisms of mono- and polysynaptic communications. Associations between the functional gradients and BMI were strongest when the hierarchical structure was the most evident. Moreover, the gradient-BMI association map was related to the microstructural features, and the findings indicated that the BMI-related structure-function coupling was significantly associated with brain microstructure, particularly in higher-order transmodal areas. Finally, transcriptomic association analysis revealed the potential biological underpinnings specifying gene enrichment in the striatum, hypothalamus, and cortical cells. Our findings provide evidence that structure-function correspondence is strongly coupled with BMI when hierarchical organization is the most apparent and that the associations are related to the multiscale properties of the brain, leading to an advanced understanding of the neural mechanisms related to BMI.
AbstractList •Structure-function coupling related to body mass index (BMI) was investigated.•We simulated functional connectivity from structural data using Riemannian approach.•BMI-related alterations in coupling were most clear when the hierarchy was evident.•Alterations were most obvious in the transmodal regions.•Cytoarchitecture and transcriptomic analyses provided biological underpinnings. Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with altered brain structure and function. However, the mechanism underlying the alteration of structure-function correspondence according to BMI is under-investigated. In this study, we studied structural and functional connectivity derived from diffusion MRI tractography and inter-regional correlations of functional MRI time series, respectively. We combined the structural and functional connectivity information using the Riemannian optimization approach. First, the low-dimensional principal eigenvectors (i.e., gradients) of the structural connectivity were generated by applying diffusion map embedding with varying diffusion times. A transformation was identified so that the structural and functional embeddings share the same coordinate system, and subsequently, the functional connectivity matrix was simulated. Then, we generated gradients from the simulated functional connectivity matrix. We found the most apparent cortical hierarchical organization differentiating between low-level sensory and higher-order transmodal regions in the middle of the diffusion time, indicating that the hierarchical organization of the brain may reflect the intermediate mechanisms of mono- and polysynaptic communications. Associations between the functional gradients and BMI were strongest when the hierarchical structure was the most evident. Moreover, the gradient-BMI association map was related to the microstructural features, and the findings indicated that the BMI-related structure-function coupling was significantly associated with brain microstructure, particularly in higher-order transmodal areas. Finally, transcriptomic association analysis revealed the potential biological underpinnings specifying gene enrichment in the striatum, hypothalamus, and cortical cells. Our findings provide evidence that structure-function correspondence is strongly coupled with BMI when hierarchical organization is the most apparent and that the associations are related to the multiscale properties of the brain, leading to an advanced understanding of the neural mechanisms related to BMI.
Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with altered brain structure and function. However, the mechanism underlying the alteration of structure-function correspondence according to BMI is under-investigated. In this study, we studied structural and functional connectivity derived from diffusion MRI tractography and inter-regional correlations of functional MRI time series, respectively. We combined the structural and functional connectivity information using the Riemannian optimization approach. First, the low-dimensional principal eigenvectors (i.e., gradients) of the structural connectivity were generated by applying diffusion map embedding with varying diffusion times. A transformation was identified so that the structural and functional embeddings share the same coordinate system, and subsequently, the functional connectivity matrix was simulated. Then, we generated gradients from the simulated functional connectivity matrix. We found the most apparent cortical hierarchical organization differentiating between low-level sensory and higher-order transmodal regions in the middle of the diffusion time, indicating that the hierarchical organization of the brain may reflect the intermediate mechanisms of mono- and polysynaptic communications. Associations between the functional gradients and BMI were strongest when the hierarchical structure was the most evident. Moreover, the gradient-BMI association map was related to the microstructural features, and the findings indicated that the BMI-related structure-function coupling was significantly associated with brain microstructure, particularly in higher-order transmodal areas. Finally, transcriptomic association analysis revealed the potential biological underpinnings specifying gene enrichment in the striatum, hypothalamus, and cortical cells. Our findings provide evidence that structure-function correspondence is strongly coupled with BMI when hierarchical organization is the most apparent and that the associations are related to the multiscale properties of the brain, leading to an advanced understanding of the neural mechanisms related to BMI.
Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with altered brain structure and function. However, the mechanism underlying the alteration of structure-function correspondence according to BMI is under-investigated. In this study, we studied structural and functional connectivity derived from diffusion MRI tractography and inter-regional correlations of functional MRI time series, respectively. We combined the structural and functional connectivity information using the Riemannian optimization approach. First, the low-dimensional principal eigenvectors (i.e., gradients) of the structural connectivity were generated by applying diffusion map embedding with varying diffusion times. A transformation was identified so that the structural and functional embeddings share the same coordinate system, and subsequently, the functional connectivity matrix was simulated. Then, we generated gradients from the simulated functional connectivity matrix. We found the most apparent cortical hierarchical organization differentiating between low-level sensory and higher-order transmodal regions in the middle of the diffusion time, indicating that the hierarchical organization of the brain may reflect the intermediate mechanisms of mono- and polysynaptic communications. Associations between the functional gradients and BMI were strongest when the hierarchical structure was the most evident. Moreover, the gradient-BMI association map was related to the microstructural features, and the findings indicated that the BMI-related structure-function coupling was significantly associated with brain microstructure, particularly in higher-order transmodal areas. Finally, transcriptomic association analysis revealed the potential biological underpinnings specifying gene enrichment in the striatum, hypothalamus, and cortical cells. Our findings provide evidence that structure-function correspondence is strongly coupled with BMI when hierarchical organization is the most apparent and that the associations are related to the multiscale properties of the brain, leading to an advanced understanding of the neural mechanisms related to BMI.Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with altered brain structure and function. However, the mechanism underlying the alteration of structure-function correspondence according to BMI is under-investigated. In this study, we studied structural and functional connectivity derived from diffusion MRI tractography and inter-regional correlations of functional MRI time series, respectively. We combined the structural and functional connectivity information using the Riemannian optimization approach. First, the low-dimensional principal eigenvectors (i.e., gradients) of the structural connectivity were generated by applying diffusion map embedding with varying diffusion times. A transformation was identified so that the structural and functional embeddings share the same coordinate system, and subsequently, the functional connectivity matrix was simulated. Then, we generated gradients from the simulated functional connectivity matrix. We found the most apparent cortical hierarchical organization differentiating between low-level sensory and higher-order transmodal regions in the middle of the diffusion time, indicating that the hierarchical organization of the brain may reflect the intermediate mechanisms of mono- and polysynaptic communications. Associations between the functional gradients and BMI were strongest when the hierarchical structure was the most evident. Moreover, the gradient-BMI association map was related to the microstructural features, and the findings indicated that the BMI-related structure-function coupling was significantly associated with brain microstructure, particularly in higher-order transmodal areas. Finally, transcriptomic association analysis revealed the potential biological underpinnings specifying gene enrichment in the striatum, hypothalamus, and cortical cells. Our findings provide evidence that structure-function correspondence is strongly coupled with BMI when hierarchical organization is the most apparent and that the associations are related to the multiscale properties of the brain, leading to an advanced understanding of the neural mechanisms related to BMI.
ArticleNumber 120590
Author Park, Yunseo
Kim, Chae Yeon
Namgung, Jong Young
Park, Bo-yong
Park, Yeongjun
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  fullname: Namgung, Jong Young
  organization: Department of Data Science, Inha University, Incheon, Republic of Korea
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  givenname: Yeongjun
  surname: Park
  fullname: Park, Yeongjun
  organization: Department of Electrical and Computer Engineering, Sungkyunkwan University, Suwon, Republic of Korea
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  givenname: Yunseo
  surname: Park
  fullname: Park, Yunseo
  organization: Department of Data Science, Inha University, Incheon, Republic of Korea
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  givenname: Chae Yeon
  surname: Kim
  fullname: Kim, Chae Yeon
  organization: Department of Data Science, Inha University, Incheon, Republic of Korea
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  givenname: Bo-yong
  orcidid: 0000-0001-7096-337X
  surname: Park
  fullname: Park, Bo-yong
  email: boyong.park@inha.ac.kr
  organization: Department of Data Science, Inha University, Incheon, Republic of Korea
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38548036$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_1002_hbm_70019
crossref_primary_10_1016_j_nicl_2025_103817
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Keywords Structure-function coupling
Body mass index
Diffusion time
Synaptic communication
Riemannian optimization
synaptic communication
diffusion time
body mass index
Language English
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elsevier_clinicalkey_doi_10_1016_j_neuroimage_2024_120590
PublicationCentury 2000
PublicationDate 2024-05-01
PublicationDateYYYYMMDD 2024-05-01
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  text: 2024-05-01
  day: 01
PublicationDecade 2020
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PublicationTitle NeuroImage (Orlando, Fla.)
PublicationTitleAlternate Neuroimage
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Elsevier Limited
Elsevier
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Snippet •Structure-function coupling related to body mass index (BMI) was investigated.•We simulated functional connectivity from structural data using Riemannian...
Body mass index (BMI) is an indicator of obesity, and recent neuroimaging studies have demonstrated that inter-individual variations in BMI are associated with...
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SubjectTerms Association analysis
Autism
Body mass index
Brain architecture
Communication
Diffusion time
Drug use
Eigenvectors
Embedding
Functional anatomy
Functional magnetic resonance imaging
Gene expression
Hypothalamus
Magnetic resonance imaging
Mental disorders
Metabolism
Neostriatum
Neural networks
Neuroimaging
Obesity
Optimization
Riemannian optimization
Structure-function coupling
Structure-function relationships
Synaptic communication
Transcriptomics
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Title Diffusion time-related structure-function coupling reveals differential association with inter-individual variations in body mass index
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