Cortical reorganization in central cord syndrome versus asymptomatic spinal cord compression: a cross-sectional fNIRS study on upper limb motor function

The severity of spinal cord compression does not fully explain the heterogeneity of upper limb motor impairment in Traumatic Central Cord Syndrome (TCCS). This study aimed to decouple the neuroimaging signatures of anatomical compression from symptomatic functional failure by investigating supraspinal reorganization in TCCS compared to Asymptomatic Cervical Spinal Cord Compression (ACSCC). We recruited 20 patients with TCCS, 20 subjects with ACSCC, and 20 healthy controls (HC). Cortical hemodynamics were recorded using functional near-infrared spectroscopy (fNIRS) during resting-state and a self-paced finger-tapping task. Clinical impairments were assessed using the Neck Disability Index (NDI) and modified Japanese Orthopaedic Association (mJOA) scale. Behaviorally, ACSCC subjects maintained clinical equivalence to HCs (all p > 0.05), whereas the TCCS group exhibited severe functional deterioration (all p < 0.001). Neuroimaging revealed that the ACSCC group preserved robust resting-state functional connectivity (rs-FC) and task-evoked activation comparable to HCs (FDR-corrected p > 0.05). In stark contrast, the TCCS group demonstrated profound rs-FC decoupling between the sensorimotor and prefrontal networks (FDR-corrected p < 0.01). During motor execution, TCCS patients exhibited a widespread recruitment failure in higher-order cortical regions, including the supplementary motor area (SMA, FDR-corrected p = 0.0055) and dorsolateral prefrontal cortex (DLPFC, FDR-corrected p = 0.0021). Crucially, robust brain-behavior correlations (confirmed via 5,000 bootstrap resamples) revealed that attenuated activation in the higher-order regions was significantly associated with worse NDI and mJOA scores (adjusted p < 0.05). The distinct cortical profiles between cohorts suggest a conceptual shift from neural compensation in the asymptomatic phase to “cortical exhaustion” in the symptomatic phase. The profound failure of top-down prefrontal-motor drive within higher-order networks may represent a key supraspinal mechanism underlying fine motor deficits in TCCS, highlighting the DLPFC and SMA as promising targets for non-invasive brain stimulation.