Learning divisive normalization in primary visual cortex

Divisive normalization (DN) is a prominent computational building block in the brain that has been proposed as a canonical cortical operation. Numerous experimental studies have verified its importance for capturing nonlinear neural response properties to simple, artificial stimuli, and computational studies suggest that DN is also an important component for processing natural stimuli. However, we lack quantitative models of DN that are directly informed by measurements of spiking responses in the brain and applicable to arbitrary stimuli. Here, we propose a DN model that is applicable to arbitrary input images. We test its ability to predict how neurons in macaque primary visual cortex (V1) respond to natural images, with a focus on nonlinear response properties within the classical receptive field. Our model consists of one layer of subunits followed by learned orientation-specific DN. It outperforms linear-nonlinear and wavelet-based feature representations and makes a significant step towards the performance of state-of-the-art convolutional neural network (CNN) models. Unlike deep CNNs, our compact DN model offers a direct interpretation of the nature of normalization. By inspecting the learned normalization pool of our model, we gained insights into a long-standing question about the tuning properties of DN that update the current textbook description: we found that within the receptive field oriented features were normalized preferentially by features with similar orientation rather than non-specifically as currently assumed.Author summary: Divisive normalization (DN) is a computational building block throughout sensory processing in the brain. We currently lack an understanding of what role this normalization mechanism plays when processing complex stimuli like natural images. Here, we use modern machine learning methods to build a general DN model that is directly informed by data from primary visual cortex (V1). Contrary to high-predictive deep learning models, our DN-based model’s parameters offer a straightforward interpretation of the nature of normalization. Within the receptive field, we found that neurons responding strongly to a specific orientation are preferentially normalized by other neurons that are highly active for similar orientations, rather than being normalized by all neurons as it is currently assumed by textbook models.