The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases
Brain signal variability has been consistently linked to functional integration; however, whether this coupling is associated with cognitive functions and/or psychiatric diseases has not been clarified. Using multiple multimodality datasets, including resting-state functional magnetic resonance imag...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2021-08-01
|
| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S105381192100464X |
| _version_ | 1818623178805608448 |
|---|---|
| author | Jintao Sheng Liang Zhang Junjiao Feng Jing Liu Anqi Li Wei Chen Yuedi Shen Jinhui Wang Yong He Gui Xue |
| author_facet | Jintao Sheng Liang Zhang Junjiao Feng Jing Liu Anqi Li Wei Chen Yuedi Shen Jinhui Wang Yong He Gui Xue |
| author_sort | Jintao Sheng |
| collection | DOAJ |
| description | Brain signal variability has been consistently linked to functional integration; however, whether this coupling is associated with cognitive functions and/or psychiatric diseases has not been clarified. Using multiple multimodality datasets, including resting-state functional magnetic resonance imaging (rsfMRI) data from the Human Connectome Project (HCP: N = 927) and a Beijing sample (N = 416) and cerebral blood flow (CBF) and rsfMRI data from a Hangzhou sample (N = 29), we found that, compared with the existing variability measure (i.e., SDBOLD), the mean-scaled (standardized) fractional standard deviation of the BOLD signal (mfSDBOLD) maintained very high test-retest reliability, showed greater cross-site reliability and was less affected by head motion. We also found strong reproducible couplings between the mfSDBOLD and functional integration measured by the degree centrality (DC), both cross-voxel and cross-subject, which were robust to scanning and preprocessing parameters. Moreover, both mfSDBOLD and DC were correlated with CBF, suggesting a common physiological basis for both measures. Critically, the degree of coupling between mfSDBOLD and long-range DC was positively correlated with individuals’ cognitive total composite scores. Brain regions with greater mismatches between mfSDBOLD and long-range DC were more vulnerable to brain diseases. Our results suggest that BOLD signal variability could serve as a meaningful index of local function that underlies functional integration in the human brain and that a strong coupling between BOLD signal variability and functional integration may serve as a hallmark of balanced brain networks that are associated with optimal brain functions. |
| first_indexed | 2024-12-16T18:36:56Z |
| format | Article |
| id | doaj.art-f1fbda5bbd854f71812643dfcde58f77 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-16T18:36:56Z |
| publishDate | 2021-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-f1fbda5bbd854f71812643dfcde58f772022-12-21T22:21:09ZengElsevierNeuroImage1095-95722021-08-01237118187The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseasesJintao Sheng0Liang Zhang1Junjiao Feng2Jing Liu3Anqi Li4Wei Chen5Yuedi Shen6Jinhui Wang7Yong He8Gui Xue9State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaDepartment of Psychiatry, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, and the Collaborative Innovation Center for Brain Science, Hangzhou, Zhejiang 310000, PR ChinaThe Affiliated Hospital of Hangzhou Normal University, Hangzhou Normal University, Hangzhou, Zhejiang 310000, PR ChinaGuangdong Key Laboratory of Mental Health and Cognitive Science, Center for Studies of Psychological Application, South China Normal University, Institute for Brain Research and Rehabilitation, Guangzhou 510631, PR China; Key Laboratory of Brain, Ministry of Education, Cognition and Education Sciences (South China Normal University), PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR ChinaState Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR China; Corresponding author.Brain signal variability has been consistently linked to functional integration; however, whether this coupling is associated with cognitive functions and/or psychiatric diseases has not been clarified. Using multiple multimodality datasets, including resting-state functional magnetic resonance imaging (rsfMRI) data from the Human Connectome Project (HCP: N = 927) and a Beijing sample (N = 416) and cerebral blood flow (CBF) and rsfMRI data from a Hangzhou sample (N = 29), we found that, compared with the existing variability measure (i.e., SDBOLD), the mean-scaled (standardized) fractional standard deviation of the BOLD signal (mfSDBOLD) maintained very high test-retest reliability, showed greater cross-site reliability and was less affected by head motion. We also found strong reproducible couplings between the mfSDBOLD and functional integration measured by the degree centrality (DC), both cross-voxel and cross-subject, which were robust to scanning and preprocessing parameters. Moreover, both mfSDBOLD and DC were correlated with CBF, suggesting a common physiological basis for both measures. Critically, the degree of coupling between mfSDBOLD and long-range DC was positively correlated with individuals’ cognitive total composite scores. Brain regions with greater mismatches between mfSDBOLD and long-range DC were more vulnerable to brain diseases. Our results suggest that BOLD signal variability could serve as a meaningful index of local function that underlies functional integration in the human brain and that a strong coupling between BOLD signal variability and functional integration may serve as a hallmark of balanced brain networks that are associated with optimal brain functions.http://www.sciencedirect.com/science/article/pii/S105381192100464XResting-state fMRIMean-scaled fractional BOLD signal variabilityDegree centralityCognitive functionDisease vulnerability |
| spellingShingle | Jintao Sheng Liang Zhang Junjiao Feng Jing Liu Anqi Li Wei Chen Yuedi Shen Jinhui Wang Yong He Gui Xue The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases NeuroImage Resting-state fMRI Mean-scaled fractional BOLD signal variability Degree centrality Cognitive function Disease vulnerability |
| title | The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| title_full | The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| title_fullStr | The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| title_full_unstemmed | The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| title_short | The coupling of BOLD signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| title_sort | coupling of bold signal variability and degree centrality underlies cognitive functions and psychiatric diseases |
| topic | Resting-state fMRI Mean-scaled fractional BOLD signal variability Degree centrality Cognitive function Disease vulnerability |
| url | http://www.sciencedirect.com/science/article/pii/S105381192100464X |
| work_keys_str_mv | AT jintaosheng thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT liangzhang thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT junjiaofeng thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT jingliu thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT anqili thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT weichen thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT yuedishen thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT jinhuiwang thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT yonghe thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT guixue thecouplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT jintaosheng couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT liangzhang couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT junjiaofeng couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT jingliu couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT anqili couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT weichen couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT yuedishen couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT jinhuiwang couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT yonghe couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases AT guixue couplingofboldsignalvariabilityanddegreecentralityunderliescognitivefunctionsandpsychiatricdiseases |