Relationships Between Intra-Spinal Resting-State Functional Connectivity and Electrophysiology Following Spinal Cord Injury

We previously reported that a unilateral dorsal column lesion (DCL) at the cervical C4 level primarily reduces inter-horn resting-state functional connectivity (rsFC) measured by functional Magnetic Resonance Imaging (fMRI) in segments below the lesion. This study compares changes in rsFC from fMRI with changes in local field potential (LFP) coherence over an extended post-injury period. High-resolution fMRI and LFP data were acquired bilaterally in healthy monkeys and at 3- and 6-months post-lesion. At 3 months post-injury, tactile-stimulus-evoked LFP power in the dorsal horn was significantly weaker than in the healthy cord and non-lesion side. LFP coherences increased on the lesion side for the dorsal-to-intermediate zone (D-IGM) and dorsal-to-ventral (D-V) pairs but decreased for the non-lesion side D-IGM. By 6 months, stimulus-evoked LFP power on the lesion side remained low. LFP coherences between dorsal-to-dorsal (D-D), ventral-to-ventral (V-V), and D-V pairs on both the lesion and non-lesion sides were significantly reduced relative to the healthy cord. Low-frequency (delta, theta, and alpha) D-IGM coherences on the lesion side, and high-frequency (beta and gamma) coherences on the non-lesion side, were also significantly weakened. Across specific inter-horn pairs and time points, changes in LFP coherences and rsFC measures were weakly correlated. Measurements of inter-horn correlations two segments caudal to the lesion level at C7 revealed distance-dependent intraspinal connectivity changes following DCL. Post-mortem histology confirmed a complete DCL in most animals (7/9). The extent of the disruption of ascending sensory afferents, as assessed histologically, did not appear to correlate with the degree of LFP power reduction or rsFC changes at post-injury time points. In summary, we observed temporally and spatially heterogeneous changes of fMRI correlations and LFP coherences within intraspinal circuits. fMRI rsFC and LFP coherences were not always concordant, with discrepancies depending on specific gray-matter horns and intermediate-zone pairs.