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 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.