Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities
Resting state functional MRI (rsfMRI) exploits variations in blood-oxygenation-level-dependent (BOLD) signals to infer resting state functional connectivity (FC) within and between brain networks. However, there have been few reports quantifying and validating the results of rsfMRI analyses with oth...
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| Format: | Article |
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Elsevier
2025-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158225000233 |
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| author | Anirban Sengupta Pai-Feng Yang Jamie L. Reed Arabinda Mishra Feng Wang Isaac V Manzanera Esteve Zhangyan Yang Li Min Chen John C. Gore |
| author_facet | Anirban Sengupta Pai-Feng Yang Jamie L. Reed Arabinda Mishra Feng Wang Isaac V Manzanera Esteve Zhangyan Yang Li Min Chen John C. Gore |
| author_sort | Anirban Sengupta |
| collection | DOAJ |
| description | Resting state functional MRI (rsfMRI) exploits variations in blood-oxygenation-level-dependent (BOLD) signals to infer resting state functional connectivity (FC) within and between brain networks. However, there have been few reports quantifying and validating the results of rsfMRI analyses with other metrics of brain circuits. We measured longitudinal changes in FC both within and between brain networks in three squirrel monkeys after focal lesions of the thalamic ventroposterior lateral nucleus (VPL) that were intended to disrupt the input to somatosensory cortex and impair manual dexterity. Local field potential signals were recorded to assess electrophysiological changes during each animal’s recovery, and behavioral performances were measured longitudinally using a sugar-pellet grasping task. Finally, end-point histological evaluations were performed on brain tissue slices to quantify the VPL damage. The rsfMRI data analysis showed significant decrease in FC measures both within and between networks immediately post-injury, which started to recover at different time-points for each animal. The trajectories of FC recovery for each animal mirrored their individual behavioral recovery time-courses. Electrophysiological measurements of inter-electrode coherences and end-point histological measures also aligned well with the graded injury effects measured using rsfMRI-based FC. A simple algorithm employing FC measures from the somatosensory network could accurately predict each monkeys’ behavioral recovery timeframe after four weeks post-injury. Whole brain between-network FC measures further revealed that the injury effects were not limited to thalamocortical connections but were rather more widespread. Overall, this study provides evidence of the validity of rsfMRI based FC measures as indicators of the functional integrity and behavioral relevance following an injury to a specific brain circuit. |
| format | Article |
| id | doaj-art-9b8d9d235d9e4cc6a19b663236fdeb90 |
| institution | DOAJ |
| issn | 2213-1582 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj-art-9b8d9d235d9e4cc6a19b663236fdeb902025-08-20T02:57:32ZengElsevierNeuroImage: Clinical2213-15822025-01-014510375310.1016/j.nicl.2025.103753Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activitiesAnirban Sengupta0Pai-Feng Yang1Jamie L. Reed2Arabinda Mishra3Feng Wang4Isaac V Manzanera Esteve5Zhangyan Yang6Li Min Chen7John C. Gore8Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USA; Corresponding author at: Department of Radiology and Radiological Sciences, Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, 1161 21st Ave S, MCN AA1105, Nashville, TN 37232, USA.Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USADepartment of Plastic Surgery, Vanderbilt University Medical Center, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Biomedical Engineering, Vanderbilt University, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USA; Department of Biomedical Engineering, Vanderbilt University, USAVanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, USA; Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, USA; Department of Biomedical Engineering, Vanderbilt University, USA; Department of Physics and Astronomy, Vanderbilt University, USAResting state functional MRI (rsfMRI) exploits variations in blood-oxygenation-level-dependent (BOLD) signals to infer resting state functional connectivity (FC) within and between brain networks. However, there have been few reports quantifying and validating the results of rsfMRI analyses with other metrics of brain circuits. We measured longitudinal changes in FC both within and between brain networks in three squirrel monkeys after focal lesions of the thalamic ventroposterior lateral nucleus (VPL) that were intended to disrupt the input to somatosensory cortex and impair manual dexterity. Local field potential signals were recorded to assess electrophysiological changes during each animal’s recovery, and behavioral performances were measured longitudinally using a sugar-pellet grasping task. Finally, end-point histological evaluations were performed on brain tissue slices to quantify the VPL damage. The rsfMRI data analysis showed significant decrease in FC measures both within and between networks immediately post-injury, which started to recover at different time-points for each animal. The trajectories of FC recovery for each animal mirrored their individual behavioral recovery time-courses. Electrophysiological measurements of inter-electrode coherences and end-point histological measures also aligned well with the graded injury effects measured using rsfMRI-based FC. A simple algorithm employing FC measures from the somatosensory network could accurately predict each monkeys’ behavioral recovery timeframe after four weeks post-injury. Whole brain between-network FC measures further revealed that the injury effects were not limited to thalamocortical connections but were rather more widespread. Overall, this study provides evidence of the validity of rsfMRI based FC measures as indicators of the functional integrity and behavioral relevance following an injury to a specific brain circuit.http://www.sciencedirect.com/science/article/pii/S2213158225000233ThalamusfMRIFunctional ConnectivityVPL |
| spellingShingle | Anirban Sengupta Pai-Feng Yang Jamie L. Reed Arabinda Mishra Feng Wang Isaac V Manzanera Esteve Zhangyan Yang Li Min Chen John C. Gore Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities NeuroImage: Clinical Thalamus fMRI Functional Connectivity VPL |
| title | Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities |
| title_full | Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities |
| title_fullStr | Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities |
| title_full_unstemmed | Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities |
| title_short | Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities |
| title_sort | correspondence between thalamic injury induced changes in resting state fmri of monkeys and their sensorimotor behaviors and neural activities |
| topic | Thalamus fMRI Functional Connectivity VPL |
| url | http://www.sciencedirect.com/science/article/pii/S2213158225000233 |
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