How brain structure–function decoupling supports individual cognition and its molecular mechanism
Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region‐specific and hierarchical across the neocortex. However, the relationship between hierarchical structur...
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| Published in | Human brain mapping Vol. 45; no. 2; pp. e26575 - n/a |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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Hoboken, USA
John Wiley & Sons, Inc
01.02.2024
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| Abstract | Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region‐specific and hierarchical across the neocortex. However, the relationship between hierarchical structure–function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure–function decoupling remain incompletely characterized. Here, we used the structural‐decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region‐specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high‐level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor‐related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure–function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure–function decoupling.
Practitioner Points
Structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks.
High‐level hierarchical structure–function decoupling contributes much more than low‐level decoupling to individual cognition.
Structure–function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility.
The distribution of structure–function decoupling is hierarchical across the neocortex (a, b) and high‐level hierarchical structure–function decoupling contributes much more than low‐level decoupling to individual cognition (c, d). Structure–function decoupling was associated with receptor‐related gene terms (e) and four neurotransmitter receptors/transporters (f). |
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| AbstractList | Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region-specific and hierarchical across the neocortex. However, the relationship between hierarchical structure-function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure-function decoupling remain incompletely characterized. Here, we used the structural-decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region-specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high-level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor-related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure-function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure-function decoupling. PRACTITIONER POINTS: Structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. High-level hierarchical structure-function decoupling contributes much more than low-level decoupling to individual cognition. Structure-function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility.Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region-specific and hierarchical across the neocortex. However, the relationship between hierarchical structure-function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure-function decoupling remain incompletely characterized. Here, we used the structural-decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region-specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high-level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor-related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure-function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure-function decoupling. PRACTITIONER POINTS: Structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. High-level hierarchical structure-function decoupling contributes much more than low-level decoupling to individual cognition. Structure-function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility. Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region‐specific and hierarchical across the neocortex. However, the relationship between hierarchical structure–function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure–function decoupling remain incompletely characterized. Here, we used the structural‐decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region‐specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high‐level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor‐related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure–function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure–function decoupling. Practitioner Points Structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. High‐level hierarchical structure–function decoupling contributes much more than low‐level decoupling to individual cognition. Structure–function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility. The distribution of structure–function decoupling is hierarchical across the neocortex (a, b) and high‐level hierarchical structure–function decoupling contributes much more than low‐level decoupling to individual cognition (c, d). Structure–function decoupling was associated with receptor‐related gene terms (e) and four neurotransmitter receptors/transporters (f). Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region-specific and hierarchical across the neocortex. However, the relationship between hierarchical structure–function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure–function decoupling remain incompletely characterized. Here, we used the structural-decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region-specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high-level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor-related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure–function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure–function decoupling.Practitioner PointsStructure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks.High-level hierarchical structure–function decoupling contributes much more than low-level decoupling to individual cognition.Structure–function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility. Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region‐specific and hierarchical across the neocortex. However, the relationship between hierarchical structure–function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure–function decoupling remain incompletely characterized. Here, we used the structural‐decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region‐specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure–function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high‐level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor‐related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure–function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure–function decoupling. The distribution of structure–function decoupling is hierarchical across the neocortex (a, b) and high‐level hierarchical structure–function decoupling contributes much more than low‐level decoupling to individual cognition (c, d). Structure–function decoupling was associated with receptor‐related gene terms (e) and four neurotransmitter receptors/transporters (f). Functional signals emerge from the structural network, supporting multiple cognitive processes through underlying molecular mechanism. The link between human brain structure and function is region-specific and hierarchical across the neocortex. However, the relationship between hierarchical structure-function decoupling and the manifestation of individual behavior and cognition, along with the significance of the functional systems involved, and the specific molecular mechanism underlying structure-function decoupling remain incompletely characterized. Here, we used the structural-decoupling index (SDI) to quantify the dependency of functional signals on the structural connectome using a significantly larger cohort of healthy subjects. Canonical correlation analysis (CCA) was utilized to assess the general multivariate correlation pattern between region-specific SDIs across the whole brain and multiple cognitive traits. Then, we predicted five composite cognitive scores resulting from multivariate analysis using SDIs in primary networks, association networks, and all networks, respectively. Finally, we explored the molecular mechanism related to SDI by investigating its genetic factors and relationship with neurotransmitter receptors/transporters. We demonstrated that structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. We revealed better performance in cognition prediction is achieved by using high-level hierarchical SDIs, with varying significance of different brain regions in predicting cognitive processes. We found that the SDIs were associated with the gene expression level of several receptor-related terms, and we also found the spatial distributions of four receptors/transporters significantly correlated with SDIs, namely D2, NET, MOR, and mGluR5, which play an important role in the flexibility of neuronal function. Collectively, our findings corroborate the association between hierarchical macroscale structure-function decoupling and individual cognition and provide implications for comprehending the molecular mechanism of structure-function decoupling. PRACTITIONER POINTS: Structure-function decoupling is hierarchical across the neocortex, spanning from primary networks to association networks. High-level hierarchical structure-function decoupling contributes much more than low-level decoupling to individual cognition. Structure-function decoupling could be regulated by genes associated with pivotal receptors that are crucial for neuronal function flexibility. |
| Author | Zeng, Debin Dong, Xiaoxi Wang, Xuetong Chu, Lei Li, Shuyu He, Yirong Li, Qiongling Zhao, Kun |
| AuthorAffiliation | 5 School of Artificial Intelligence Beijing University of Posts and Telecommunications Beijing China 4 Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science & Medical Engineering Beihang University Beijing China 1 State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University Beijing China 2 Beijing Key Laboratory of Brain Imaging and Connectomics Beijing Normal University Beijing China 3 IDG/McGovern Institute for Brain Research Beijing Normal University Beijing China |
| AuthorAffiliation_xml | – name: 5 School of Artificial Intelligence Beijing University of Posts and Telecommunications Beijing China – name: 2 Beijing Key Laboratory of Brain Imaging and Connectomics Beijing Normal University Beijing China – name: 3 IDG/McGovern Institute for Brain Research Beijing Normal University Beijing China – name: 4 Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science & Medical Engineering Beihang University Beijing China – name: 1 State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University Beijing China |
| Author_xml | – sequence: 1 givenname: Xiaoxi surname: Dong fullname: Dong, Xiaoxi organization: Beijing Normal University – sequence: 2 givenname: Qiongling surname: Li fullname: Li, Qiongling organization: Beijing Normal University – sequence: 3 givenname: Xuetong surname: Wang fullname: Wang, Xuetong organization: Beijing Normal University – sequence: 4 givenname: Yirong surname: He fullname: He, Yirong organization: Beijing Normal University – sequence: 5 givenname: Debin surname: Zeng fullname: Zeng, Debin organization: Beihang University – sequence: 6 givenname: Lei surname: Chu fullname: Chu, Lei organization: Beihang University – sequence: 7 givenname: Kun surname: Zhao fullname: Zhao, Kun organization: Beijing University of Posts and Telecommunications – sequence: 8 givenname: Shuyu orcidid: 0000-0002-3459-6821 surname: Li fullname: Li, Shuyu email: shuyuli@bnu.edu.cn organization: Beijing Normal University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38339909$$D View this record in MEDLINE/PubMed |
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| Keywords | cortical hierarchy structure-function decoupling cognition genes neurotransmitters |
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| PublicationYear | 2024 |
| Publisher | John Wiley & Sons, Inc |
| Publisher_xml | – name: John Wiley & Sons, Inc |
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| SubjectTerms | Behavior Brain Cerebral cortex Cognition Cognition & reasoning Cognitive ability Communication Correlation analysis cortical hierarchy Decoupling Flexibility Fourier transforms Functional anatomy Gene expression genes Genetic factors Glutamic acid receptors (metabotropic) Molecular modelling Molecular structure Multivariate analysis Neocortex Networks Neurotransmitter receptors neurotransmitters Receptor mechanisms Receptors Signal processing Spatial distribution Structure-function relationships structure–function decoupling |
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| Title | How brain structure–function decoupling supports individual cognition and its molecular mechanism |
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