Anirban Sengupta , Pai-Feng Yang , Jamie L. Reed , Arabinda Mishra , Feng Wang , Isaac V Manzanera Esteve , Zhangyan Yang , Li Min Chen , John C. Gore
{"title":"Correspondence between thalamic injury-induced changes in resting-state fMRI of monkeys and their sensorimotor behaviors and neural activities","authors":"Anirban Sengupta , Pai-Feng Yang , Jamie L. Reed , Arabinda Mishra , Feng Wang , Isaac V Manzanera Esteve , Zhangyan Yang , Li Min Chen , John C. Gore","doi":"10.1016/j.nicl.2025.103753","DOIUrl":null,"url":null,"abstract":"<div><div>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.</div></div>","PeriodicalId":54359,"journal":{"name":"Neuroimage-Clinical","volume":"45 ","pages":"Article 103753"},"PeriodicalIF":3.4000,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuroimage-Clinical","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2213158225000233","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
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.
期刊介绍:
NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging.
The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.