High spatial correspondence at a columnar level between activation and resting state fMRI signals and local field potentials

Significance We found that blood oxygenation level-dependent (BOLD) signal changes within single-digit representation columns in the primary somatosensory cortices of areas 3b and 1 aligned spatially very closely with local field potential (LFP) signals in response to tactile stimulation. Moreover, resting state BOLD fMRI and LFP signals also exhibited very similar intervoxel spatial correlation profiles. These findings indicate that at a columnar level, BOLD signals faithfully reflect underlying neuronal activity both during information processing and at rest. Importantly, the spread of BOLD activity and correlations at high field are no greater than the extent of LFP signals. These results demonstrate that high-field fMRI has the ability to delineate brain activity at the columnar level, and BOLD signals faithfully reflect electrophysiological activity. Although blood oxygenation level-dependent (BOLD) fMRI has been widely used to map brain responses to external stimuli and to delineate functional circuits at rest, the extent to which BOLD signals correlate spatially with underlying neuronal activity, the spatial relationships between stimulus-evoked BOLD activations and local correlations of BOLD signals in a resting state, and whether these spatial relationships vary across functionally distinct cortical areas are not known. To address these critical questions, we directly compared the spatial extents of stimulated activations and the local profiles of intervoxel resting state correlations for both high-resolution BOLD at 9.4 T and local field potentials (LFPs), using 98-channel microelectrode arrays, in functionally distinct primary somatosensory areas 3b and 1 in nonhuman primates. Anatomic images of LFP and BOLD were coregistered within 0.10 mm accuracy. We found that the point spread functions (PSFs) of BOLD and LFP responses were comparable in the stimulus condition, and both estimates of activations were slightly more spatially constrained than local correlations at rest. The magnitudes of stimulus responses in area 3b were stronger than those in area 1 and extended in a medial to lateral direction. In addition, the reproducibility and stability of stimulus-evoked activation locations within and across both modalities were robust. Our work suggests that the intrinsic resolution of BOLD is not a limiting feature in practice and approaches the intrinsic precision achievable by multielectrode electrophysiology.