Deep convolutional models improve predictions of macaque V1 responses to natural images

Despite great efforts over several decades, our best models of primary visual cortex (V1) still predict spiking activity quite poorly when probed with natural stimuli, highlighting our limited understanding of the nonlinear computations in V1. Recently, two approaches based on deep learning have been successfully applied to neural data: On the one hand, transfer learning from networks trained on object recognition worked remarkably well for predicting neural responses in higher areas of the primate ventral stream, but has not yet been used to model spiking activity in early stages such as V1. On the other hand, data-driven models have been used to predict neural responses in the early visual system (retina and V1) of mice, but not primates. Here, we test the ability of both approaches to predict spiking activity in response to natural images in V1 of awake monkeys. Even though V1 is rather at an early to intermediate stage of the visual system, we found that the transfer learning approach performed similarly well to the data-driven approach and both outperformed classical linear-nonlinear and wavelet-based feature representations that build on existing theories of V1. Notably, transfer learning using a pre-trained feature space required substantially less experimental time to achieve the same performance. In conclusion, multi-layer convolutional neural networks (CNNs) set the new state of the art for predicting neural responses to natural images in primate V1 and deep features learned for object recognition are better explanations for V1 computation than all previous filter bank theories. This finding strengthens the necessity of V1 models that are multiple nonlinearities away from the image domain and it supports the idea of explaining early visual cortex based on high-level functional goals. Author summary Predicting the responses of sensory neurons to arbitrary natural stimuli is of major importance for understanding their function. Arguably the most studied cortical area is primary visual cortex (V1), where many models have been developed to explain its function. However, the most successful models built on neurophysiologists’ intuitions still fail to account for spiking responses to natural images. Here, we model spiking activity in primary visual cortex (V1) of monkeys using deep convolutional neural networks (CNNs), which have been successful in computer vision. We both trained CNNs directly to fit the data, and used CNNs trained to solve a high-level task (object categorization). With these approaches, we are able to outperform previous models and improve the state of the art in predicting the responses of early visual neurons to natural images. Our results have two important implications. First, since V1 is the result of several nonlinear stages, it should be modeled as such. Second, functional models of entire visual pathways, of which V1 is an early stage, do not only account for higher areas of such pathways, but also provide useful representations for V1 predictions.