Learning a compact representation of history is critical for planning and generalization in partially observable environments. While meta-reinforcement learning (RL) agents can attain near Bayes-optimal policies, they often fail to learn the compact, interpretable Bayes-optimal belief states. This representational inefficiency potentially limits the agent's adaptability and generalization capacity. Inspired by predictive coding in neuroscience---which suggests that the brain predicts sensory inputs as a neural implementation of Bayesian inference---and by auxiliary predictive objectives in deep RL, we investigate whether integrating self-supervised predictive coding modules into meta-RL can facilitate learning of Bayes-optimal representations. Through state machine simulation, we show that meta-RL with predictive modules consistently generates more interpretable representations that better approximate Bayes-optimal belief states compared to conventional meta-RL across a wide variety of tasks, even when both achieve optimal policies. In challenging tasks requiring active information seeking, only meta-RL with predictive modules successfully learns optimal representations and policies, whereas conventional meta-RL struggles with inadequate representation learning. Finally, we demonstrate that better representation learning leads to improved generalization. Our results strongly suggest the role of predictive learning as a guiding principle for effective representation learning in agents navigating partial observability.

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 \textit{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.

Transferring knowledge embedded in trained neural networks is a core problem in areas like model compression and continual learning. Among knowledge transfer approaches, functional transfer methods such as knowledge distillation and representational distance learning are particularly promising, since they allow for transferring knowledge across different architectures and tasks. Considering various characteristics of networks that are desirable to transfer, equivariance is a notable property that enables a network to capture valuable relationships in the data. We assess existing functional transfer methods on their ability to transfer equivariance and empirically show that they fail to even transfer shift equivariance, one of the simplest equivariances. Further theoretical analysis demonstrates that representational similarity methods, in fact, cannot guarantee the transfer of the intended equivariance. Motivated by these findings, we develop a novel transfer method that learns an equivariance model from a given teacher network and encourages the student network to acquire the same equivariance, via regularization. Experiments show that our method successfully transfers equivariance even in cases where highly restrictive methods, such as directly matching student and teacher representations, fail.

We present a joint deep neural system identification model for two major sources of neural variability: stimulus-driven and stimulus-conditioned fluctuations. To this end, we combine (1) state-of-the-art deep networks for stimulus-driven activity and (2) a flexible, normalizing flow-based generative model to capture the stimulus-conditioned variability including noise correlations. This allows us to train the model end-to-end without the need for sophisticated probabilistic approximations associated with many latent state models for stimulus-conditioned fluctuations. We train the model on the responses of thousands of neurons from multiple areas of the mouse visual cortex to natural images. We show that our model outperforms previous state-of-the-art models in predicting the distribution of neural population responses to novel stimuli, including shared stimulus-conditioned variability. Furthermore, it successfully learns known latent factors of the population responses that are related to behavioral variables such as pupil dilation, and other factors that vary systematically with brain area or retinotopic location. Overall, our model accurately accounts for two critical sources of neural variability while avoiding several complexities associated with many existing latent state models. It thus provides a useful tool for uncovering the interplay between different factors that contribute to variability in neural activity.

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.

Despite impressive performance on numerous visual tasks, Convolutional Neural Networks (CNNs) --- unlike brains --- are often highly sensitive to small perturbations of their input, e.g. adversarial noise leading to erroneous decisions. We propose to regularize CNNs using large-scale neuroscience data to learn more robust neural features in terms of representational similarity. We presented natural images to mice and measured the responses of thousands of neurons from cortical visual areas. Next, we denoised the notoriously variable neural activity using strong predictive models trained on this large corpus of responses from the mouse visual system, and calculated the representational similarity for millions of pairs of images from the model's predictions. We then used the neural representation similarity to regularize CNNs trained on image classification by penalizing intermediate representations that deviated from neural ones. This preserved performance of baseline models when classifying images under standard benchmarks, while maintaining substantially higher performance compared to baseline or control models when classifying noisy images. Moreover, the models regularized with cortical representations also improved model robustness in terms of adversarial attacks. This demonstrates that regularizing with neural data can be an effective tool to create an inductive bias towards more robust inference.

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 emerged for modeling these nonlinear computations: transfer learning from artificial neural networks trained on object recognition and data-driven convolutional neural network models trained end-to-end on large populations of neurons. Here, we test the ability of both approaches to predict spiking activity in response to natural images in V1 of awake monkeys. 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.

To better understand the representations in visual cortex, we need to generate better predictions of neural activity in awake animals presented with their ecological input: natural video. Despite recent advances in models for static images, models for predicting responses to natural video are scarce and standard linear-nonlinear models perform poorly. We developed a new deep recurrent network architecture that predicts inferred spiking activity of thousands of mouse V1 neurons simultaneously recorded with two-photon microscopy, while accounting for confounding factors such as the animal's gaze position and brain state changes related to running state and pupil dilation. Powerful system identification models provide an opportunity to gain insight into cortical functions through in silico experiments that can subsequently be tested in the brain. However, in many cases this approach requires that the model is able to generalize to stimulus statistics that it was not trained on, such as band-limited noise and other parameterized stimuli. We investigated these domain transfer properties in our model and find that our model trained on natural images is able to correctly predict the orientation tuning of neurons in responses to artificial noise stimuli. Finally, we show that we can fully generalize from movies to noise and maintain high predictive performance on both stimulus domains by fine-tuning only the final layer's weights on a network otherwise trained on natural movies. The converse, however, is not true.