Noise correlations in the human brain and their impact on pattern classification

Multivariate decoding methods, such as multivoxel pattern analysis (MVPA), are highly effective at extracting information from brain imaging data. Yet, the precise nature of the information that MVPA draws upon remains controversial. Most current theories emphasize the enhanced sensitivity imparted by aggregating across voxels that have mixed and weak selectivity. However, beyond the selectivity of individual voxels, neural variability is correlated across voxels, and such noise correlations may contribute importantly to accurate decoding. Indeed, a recent computational theory proposed that noise correlations enhance multivariate decoding from heterogeneous neural populations. Here we extend this theory from the scale of neurons to functional magnetic resonance imaging (fMRI) and show that noise correlations between heterogeneous populations of voxels (i.e., voxels selective for different stimulus variables) contribute to the success of MVPA. Specifically, decoding performance is enhanced when voxels with high vs. low noise correlations (measured during rest or in the background of the task) are selected during classifier training. Conversely, voxels that are strongly selective for one class in a GLM or that receive high classification weights in MVPA tend to exhibit high noise correlations with voxels selective for the other class being discriminated against. Furthermore, we use simulations to show that this is a general property of fMRI data and that selectivity and noise correlations can have distinguishable influences on decoding. Taken together, our findings demonstrate that if there is signal in the data, the resulting above-chance classification accuracy is modulated by the magnitude of noise correlations.Author summary: A central challenge in cognitive neuroscience is decoding mental representations from patterns of brain activity. With functional magnetic resonance imaging (fMRI), multivariate decoding methods like multivoxel pattern analysis (MVPA) have produced numerous discoveries about the brain. However, what information these methods draw upon remains the subject of debate. Typically, each voxel is thought to contribute information through its selectivity (i.e., how differently it responds to the classes being decoded), with improved sensitivity reflecting the aggregation of selectivity across voxels. We show that this interpretation downplays an important factor: MVPA is also highly attuned to noise correlations between voxels with opposite selectivity. Across several analyses of an fMRI dataset, we demonstrate a positive relationship between the magnitude of noise correlations and multivariate decoding performance. Indeed, voxels more selective for one class, or heavily weighted in MVPA, tend to be more strongly correlated with voxels selective for the opposite class. Furthermore, using a model to simulate different levels of selectivity and noise correlations, we find that the benefit of noise correlations for decoding is a general property of fMRI data. These findings help elucidate the computational underpinnings of multivariate decoding in cognitive neuroscience and provide insight into the nature of neural representations.