Understanding multivariate brain activity: Evaluating the effect of voxelwise noise correlations on population codes in functional magnetic resonance imaging

Previous studies have shown that neurons exhibit trial-by-trial correlated activity and that such noise correlations (NCs) greatly impact the accuracy of population codes. Meanwhile, multivariate pattern analysis (MVPA) has become a mainstream approach in functional magnetic resonance imaging (fMRI), but it remains unclear how NCs between voxels influence MVPA performance. Here, we tackle this issue by combining voxel-encoding modeling and MVPA. We focus on a well-established form of NC, tuning-compatible noise correlation (TCNC), whose sign and magnitude are systematically related to the tuning similarity between two units. We first replicate the classical finding that TCNCs impair population codes in a standard neuronal population. We then extend our analysis to fMRI data, and show that voxelwise TCNCs do not impair and can even improve MVPA performance when TCNCs are strong or the number of voxels is large. We also confirm these results using standard information-theoretic analyses in computational neuroscience. Further computational analyses demonstrate that the discrepancy between the effect of TCNCs in neuronal and voxel populations can be explained by tuning heterogeneity and pool sizes. Our results provide a theoretical foundation to understand the effect of correlated activity on population codes in macroscopic fMRI data. Our results also suggest that future fMRI research could benefit from a closer examination of the correlational structure of multivariate responses, which is not directly revealed by conventional MVPA approaches.