Taking the neural sampling code very seriously: A data-driven approach for evaluating generative models of the visual system

Prevailing theories of perception hypothesize that the brain implements perception via Bayesian inference in a generative model of the world. One prominent theory, the Neural Sampling Code (NSC), posits that neuronal responses to a stimulus represent samples from the posterior distribution over latent world state variables that cause the stimulus. Although theoretically elegant, NSC does not specify the exact form of the generative model or prescribe how to link the theory to recorded neuronal activity. Previous works assume simple generative models and test their qualitative agreement with neurophysiological data. Currently, there is no precise alignment of the normative theory with neuronal recordings, especially in response to natural stimuli, and a quantitative, experimental evaluation of models under NSC has been lacking. Here, we propose a novel formalization of NSC, that (a) allows us to directly fit NSC generative models to recorded neuronal activity in response to natural images, (b) formulate richer and more flexible generative models, and (c) employ standard metrics to quantitatively evaluate different generative models under NSC. Furthermore, we derive a stimulus-conditioned predictive model of neuronal responses from the trained generative model using our formalization that we compare to neural system identification models. We demonstrate our approach by fitting and comparing classical-and flexible deep learning-based generative models on population recordings from the macaque primary visual cortex (V1) to natural images, and show that the flexible models outperform classical models in both their generative-and predictive-model performance. Overall, our work is an important step towards a quantitative evaluation of NSC. It provides a framework that lets us learn the generative model directly from neuronal population recordings, paving the way for an experimentally-informed understanding of probabilistic computational principles underlying perception and behavior.