Higher-Order Convolution Improves Neural Predictivity in the Retina

Abstract: We present a novel approach to neural response prediction that incorporates higher-order operations directly within convolutional neural networks (CNNs). Our model extends traditional 3D CNNs by embedding higher-order operations within the convolutional operator itself, enabling direct modeling of multiplicative interactions between neighboring pixels across space and time. Our model increases the representational power of CNNs without increasing their depth, therefore addressing the architectural disparity between deep artificial networks and the relatively shallow processing hierarchy of biological visual systems. We evaluate our approach on two distinct datasets: salamander retinal ganglion cell (RGC) responses to natural scenes, and a new dataset of mouse RGC responses to controlled geometric transformations. Our higher-order CNN (HoCNN) achieves superior performance while requiring only half the training data compared to standard architectures, demonstrating correlation coefficients up to 0.75 with neural responses (against 0.80$\pm$0.02 retinal reliability). When integrated into state-of-the-art architectures, our approach consistently improves performance across different species and stimulus conditions. Analysis of the learned representations reveals that our network naturally encodes fundamental geometric transformations, particularly scaling parameters that characterize object expansion and contraction. This capability is especially relevant for specific cell types, such as transient OFF-alpha and transient ON cells, which are known to detect looming objects and object motion respectively, and where our model shows marked improvement in response prediction. The correlation coefficients for scaling parameters are more than twice as high in HoCNN (0.72) compared to baseline models (0.32).