Deep learning models of cognitive processes constrained by human brain connectomes

Abstract Decoding cognitive processes from recordings of brain activity has been an active topic in neuroscience research for decades. Traditional decoding studies focused on pattern classification in specific regions of interest and averaging brain activity over many trials. Recently, brain decoding with graph neural networks has been shown to scale at fine temporal resolution and on the full brain, achieving state-of-the-art performance on the human connectome project benchmark. The reason behind this success is likely the strong inductive connectome prior that enables the integration of distributed patterns of brain activity. Yet, the nature of such inductive bias is still poorly understood. In this work, we investigate the impact of the inclusion of multiple path lengths (through high-order graph convolution), the homogeneity of brain parcels (graph nodes), and the type of interactions (graph edges). We evaluate the decoding models on a large population of 1200 participants, under 21 different experimental conditions, acquired from the Human Connectome Project database. Our findings reveal that the optimal choice for large-scale cognitive decoding is to propagate neural dynamics within empirical functional connectomes and integrate brain dynamics using high-order graph convolutions. In this setting, the model exhibits high decoding accuracy and robustness against adversarial attacks on the graph architecture, including randomization in functional connectomes and lesions in targeted brain regions and networks. The trained model relies on biologically meaningful features for the prediction of cognitive states and generates task-specific graph representations resembling task-evoked activation maps. These results demonstrate that a full-brain integrative model is critical for the large-scale brain decoding. Our study establishes principles of how to effectively leverage human connectome constraints in deep graph neural networks, providing new avenues to study the neural substrates of human cognition at scale.