How environmental and physiological signals interact to influence neural circuits underlying developmentally programmed social interactions such as male territorial aggression is poorly understood. We have tested the influence of sensory cues, social context, and sex hormones on progesterone receptor (PR)-expressing neurons in the ventromedial hypothalamus (VMH) that are critical for male territorial aggression. We find that these neurons can drive aggressive displays in solitary males independent of pheromonal input, gonadal hormones, opponents, or social context. By contrast, these neurons cannot elicit aggression in socially housed males that intrude in another male’s territory unless their pheromone-sensing is disabled. This modulation of aggression cannot be accounted for by linear integration of environmental and physiological signals. Together, our studies suggest that fundamentally non-linear computations enable social context to exert a dominant influence on developmentally hard-wired hypothalamus-mediated male territorial aggression.

Understanding the circuit mechanisms of the visual code for natural scenes is a central goal of sensory neuro-science. We show that a three-layer network model predicts retinal natural scene responses with an accuracy nearing experimental limits. The model's internal structure is interpretable, as interneurons recorded separately and not modeled directly are highly correlated with model interneurons. Models fitted only to natural scenes reproduce a diverse set of phenomena related to motion encoding, adaptation, and predictive coding, establishing their ethological relevance to natural visual computation. A new approach decomposes the computations of model ganglion cells into the contributions of model interneurons, allowing automatic generation of new hypotheses for how interneurons with different spatiotemporal responses are combined to generate retinal computations, including predictive phenomena currently lacking an explanation. Our results demonstrate a unified and general approach to study the circuit mechanisms of ethological retinal computations under natural visual scenes.

The visual system processes stimuli over a wide range of spatiotemporal scales, with individual neurons receiving input from tens of thousands of neurons whose dynamics range from milliseconds to tens of seconds. This poses a challenge to create models that both accurately capture visual computations and are mechanistically interpretable. Here we present a model of salamander retinal ganglion cell spiking responses recorded with a multielectrode array that captures natural scene responses and slow adaptive dynamics. The model consists of a three-layer convolutional neural network (CNN) modified to include local recurrent synaptic dynamics taken from a linear-nonlinear-kinetic (LNK) model [1]. We presented alternating natural scenes and uniform field white noise stimuli designed to engage slow contrast adaptation. To overcome difficulties fitting slow and fast dynamics together, we first optimized all fast spatiotemporal parameters, then separately optimized recurrent slow synaptic parameters. The resulting full model reproduces a wide range of retinal computations and is mechanistically interpretable, having internal units that correspond to retinal interneurons with biophysically modeled synapses. This model allows us to study the contribution of model units to any retinal computation, and examine how long-term adaptation changes the retinal neural code for natural scenes through selective adaptation of retinal pathways.

Optimization plays a costly and crucial role in developing machine learning systems. In learned optimizers, the few hyperparameters of commonly used hand-designed optimizers, e.g. Adam or SGD, are replaced with flexible parametric functions. The parameters of these functions are then optimized so that the resulting learned optimizer minimizes a target loss on a chosen class of models. Learned optimizers can both reduce the number of required training steps and improve the final test loss. However, they can be expensive to train, and once trained can be expensive to use due to computational and memory overhead for the optimizer itself. In this work, we identify and quantify the design features governing the memory, compute, and performance trade-offs for many learned and hand-designed optimizers. We further leverage our analysis to construct a learned optimizer that is both faster and more memory efficient than previous work. Our model and training code are open source.

In this work we focus on general-purpose learned optimizers capable of training a wide variety of problems with no user-specified hyperparameters. We introduce a new, neural network parameterized, hierarchical optimizer with access to additional features such as validation loss to enable automatic regularization. Most learned optimizers have been trained on only a single task, or a small number of tasks. We train our optimizers on thousands of tasks, making use of orders of magnitude more compute, resulting in optimizers that generalize better to unseen tasks. The learned optimizers not only perform well, but learn behaviors that are distinct from existing first order optimizers. For instance, they generate update steps that have implicit regularization and adapt as the problem hyperparameters (e.g. batch size) or architecture (e.g. neural network width) change. Finally, these learned optimizers show evidence of being useful for out of distribution tasks such as training themselves from scratch.

Encoder-decoder networks with attention have proven to be a powerful way to solve many sequence-to-sequence tasks. In these networks, attention aligns encoder and decoder states and is often used for visualizing network behavior. However, the mechanisms used by networks to generate appropriate attention matrices are still mysterious. Moreover, how these mechanisms vary depending on the particular architecture used for the encoder and decoder (recurrent, feed-forward, etc.) are also not well understood. In this work, we investigate how encoder-decoder networks solve different sequence-to-sequence tasks. We introduce a way of decomposing hidden states over a sequence into temporal (independent of input) and input-driven (independent of sequence position) components. This reveals how attention matrices are formed: depending on the task requirements, networks rely more heavily on either the temporal or input-driven components. These findings hold across both recurrent and feed-forward architectures despite their differences in forming the temporal components. Overall, our results provide new insight into the inner workings of attention-based encoder-decoder networks.

Despite the widespread application of recurrent neural networks (RNNs) across a variety of tasks, a unified understanding of how RNNs solve these tasks remains elusive. In particular, it is unclear what dynamical patterns arise in trained RNNs, and how those patterns depend on the training dataset or task. This work addresses these questions in the context of a specific natural language processing task: text classification. Using tools from dynamical systems analysis, we study recurrent networks trained on a battery of both natural and synthetic text classification tasks. We find the dynamics of these trained RNNs to be both interpretable and low-dimensional. Specifically, across architectures and datasets, RNNs accumulate evidence for each class as they process the text, using a low-dimensional attractor manifold as the underlying mechanism. Moreover, the dimensionality and geometry of the attractor manifold are determined by the structure of the training dataset; in particular, we describe how simple word-count statistics computed on the training dataset can be used to predict these properties. Our observations span multiple architectures and datasets, reflecting a common mechanism RNNs employ to perform text classification. To the degree that integration of evidence towards a decision is a common computational primitive, this work lays the foundation for using dynamical systems techniques to study the inner workings of RNNs.

We present TaskSet, a dataset of tasks for use in training and evaluating optimizers. TaskSet is unique in its size and diversity, containing over a thousand tasks ranging from image classification with fully connected or convolutional neural networks, to variational autoencoders, to non-volume preserving flows on a variety of datasets. As an example application of such a dataset we explore meta-learning an ordered list of hyperparameters to try sequentially. By learning this hyperparameter list from data generated using TaskSet we achieve large speedups in sample efficiency over random search. Next we use the diversity of the TaskSet and our method for learning hyperparameter lists to empirically explore the generalization of these lists to new optimization tasks in a variety of settings including ImageNet classification with Resnet50 and LM1B language modeling with transformers. As part of this work we have opensourced code for all tasks, as well as ~29 million training curves for these problems and the corresponding hyperparameters.

Learned optimizers are increasingly effective, with performance exceeding that of hand designed optimizers such as Adam~\citep{kingma2014adam} on specific tasks \citep{metz2019understanding}. Despite the potential gains available, in current work the meta-training (or `outer-training') of the learned optimizer is performed by a hand-designed optimizer, or by an optimizer trained by a hand-designed optimizer \citep{metz2020tasks}. We show that a population of randomly initialized learned optimizers can be used to train themselves from scratch in an online fashion, without resorting to a hand designed optimizer in any part of the process. A form of population based training is used to orchestrate this self-training. Although the randomly initialized optimizers initially make slow progress, as they improve they experience a positive feedback loop, and become rapidly more effective at training themselves. We believe feedback loops of this type, where an optimizer improves itself, will be important and powerful in the future of machine learning. These methods not only provide a path towards increased performance, but more importantly relieve research and engineering effort.

Learned optimizers are algorithms that can themselves be trained to solve optimization problems. In contrast to baseline optimizers (such as momentum or Adam) that use simple update rules derived from theoretical principles, learned optimizers use flexible, high-dimensional, nonlinear parameterizations. Although this can lead to better performance in certain settings, their inner workings remain a mystery. How is a learned optimizer able to outperform a well tuned baseline? Has it learned a sophisticated combination of existing optimization techniques, or is it implementing completely new behavior? In this work, we address these questions by careful analysis and visualization of learned optimizers. We study learned optimizers trained from scratch on three disparate tasks, and discover that they have learned interpretable mechanisms, including: momentum, gradient clipping, learning rate schedules, and a new form of learning rate adaptation. Moreover, we show how the dynamics of learned optimizers enables these behaviors. Our results help elucidate the previously murky understanding of how learned optimizers work, and establish tools for interpreting future learned optimizers.

Much as replacing hand-designed features with learned functions has revolutionized how we solve perceptual tasks, we believe learned algorithms will transform how we train models. In this work we focus on general-purpose learned optimizers capable of training a wide variety of problems with no user-specified hyperparameters. We introduce a new, neural network parameterized, hierarchical optimizer with access to additional features such as validation loss to enable automatic regularization. Most learned optimizers have been trained on only a single task, or a small number of tasks. We train our optimizers on thousands of tasks, making use of orders of magnitude more compute, resulting in optimizers that generalize better to unseen tasks. The learned optimizers not only perform well, but learn behaviors that are distinct from existing first order optimizers. For instance, they generate update steps that have implicit regularization and adapt as the problem hyperparameters (e.g. batch size) or architecture (e.g. neural network width) change. Finally, these learned optimizers show evidence of being useful for out of distribution tasks such as training themselves from scratch.

Neural networks have a remarkable capacity for contextual processing--using recent or nearby inputs to modify processing of current input. For example, in natural language, contextual processing is necessary to correctly interpret negation (e.g. phrases such as "not bad"). However, our ability to understand how networks process context is limited. Here, we propose general methods for reverse engineering recurrent neural networks (RNNs) to identify and elucidate contextual processing. We apply these methods to understand RNNs trained on sentiment classification. This analysis reveals inputs that induce contextual effects, quantifies the strength and timescale of these effects, and identifies sets of these inputs with similar properties. Additionally, we analyze contextual effects related to differential processing of the beginning and end of documents. Using the insights learned from the RNNs we improve baseline Bag-of-Words models with simple extensions that incorporate contextual modification, recovering greater than 90% of the RNN's performance increase over the baseline. This work yields a new understanding of how RNNs process contextual information, and provides tools that should provide similar insight more broadly.

We present TaskSet, a dataset of tasks for use in training and evaluating optimizers. TaskSet is unique in its size and diversity, containing over a thousand tasks ranging from image classification with fully connected or convolutional neural networks, to variational autoencoders, to non-volume preserving flows on a variety of datasets. As an example application of such a dataset we explore meta-learning an ordered list of hyperparameters to try sequentially. By learning this hyperparameter list from data generated using TaskSet we achieve large speedups in sample efficiency over random search. Next we use the diversity of the TaskSet and our method for learning hyperparameter lists to empirically explore the generalization of these lists to new optimization tasks in a variety of settings including ImageNet classification with Resnet50 and LM1B language modeling with transformers. As part of this work we have opensourced code for all tasks, as well as ~29 million training curves for these problems and the corresponding hyperparameters.

Task-based modeling with recurrent neural networks (RNNs) has emerged as a popular way to infer the computational function of different brain regions. These models are quantitatively assessed by comparing the low-dimensional neural representations of the model with the brain, for example using canonical correlation analysis (CCA). However, the nature of the detailed neurobiological inferences one can draw from such efforts remains elusive. For example, to what extent does training neural networks to solve common tasks uniquely determine the network dynamics, independent of modeling architectural choices? Or alternatively, are the learned dynamics highly sensitive to different model choices? Knowing the answer to these questions has strong implications for whether and how we should use task-based RNN modeling to understand brain dynamics. To address these foundational questions, we study populations of thousands of networks, with commonly used RNN architectures, trained to solve neuroscientifically motivated tasks and characterize their nonlinear dynamics. We find the geometry of the RNN representations can be highly sensitive to different network architectures, yielding a cautionary tale for measures of similarity that rely on representational geometry, such as CCA. Moreover, we find that while the geometry of neural dynamics can vary greatly across architectures, the underlying computational scaffold-the topological structure of fixed points, transitions between them, limit cycles, and linearized dynamics-often appears universal across all architectures.

Recently, deep feedforward neural networks have achieved considerable success in modeling biological sensory processing, in terms of reproducing the input-output map of sensory neurons. However, such models raise profound questions about the very nature of explanation in neuroscience. Are we simply replacing one complex system (a biological circuit) with another (a deep network), without understanding either? Moreover, beyond neural representations, are the deep network's computational mechanisms for generating neural responses the same as those in the brain? Without a systematic approach to extracting and understanding computational mechanisms from deep neural network models, it can be difficult both to assess the degree of utility of deep learning approaches in neuroscience, and to extract experimentally testable hypotheses from deep networks. We develop such a systematic approach by combining dimensionality reduction and modern attribution methods for determining the relative importance of interneurons for specific visual computations. We apply this approach to deep network models of the retina, revealing a conceptual understanding of how the retina acts as a predictive feature extractor that signals deviations from expectations for diverse spatiotemporal stimuli. For each stimulus, our extracted computational mechanisms are consistent with prior scientific literature, and in one case yields a new mechanistic hypothesis. Thus overall, this work not only yields insights into the computational mechanisms underlying the striking predictive capabilities of the retina, but also places the framework of deep networks as neuroscientific models on firmer theoretical foundations, by providing a new roadmap to go beyond comparing neural representations to extracting and understand computational mechanisms.

Many applications in machine learning require optimizing a function whose true gradient is unknown, but where surrogate gradient information (directions that may be correlated with, but not necessarily identical to, the true gradient) is available instead. This arises when an approximate gradient is easier to compute than the full gradient (e.g. in meta-learning or unrolled optimization), or when a true gradient is intractable and is replaced with a surrogate (e.g. in certain reinforcement learning applications, or when using synthetic gradients). We propose Guided Evolutionary Strategies, a method for optimally using surrogate gradient directions along with random search. We define a search distribution for evolutionary strategies that is elongated along a guiding subspace spanned by the surrogate gradients. This allows us to estimate a descent direction which can then be passed to a first-order optimizer. We analytically and numerically characterize the tradeoffs that result from tuning how strongly the search distribution is stretched along the guiding subspace, and we use this to derive a setting of the hyperparameters that works well across problems. Finally, we apply our method to example problems, demonstrating an improvement over both standard evolutionary strategies and first-order methods (that directly follow the surrogate gradient). We provide a demo of Guided ES at https://github.com/brain-research/guided-evolutionary-strategies

The question of how neurons embedded in a network update their synaptic weights to collectively achieve behavioral goals is a longstanding problem in systems neuroscience. Since Hebb’s hypothesis [10] that cells that fire together strengthen their connections, cellular studies [6] have shed light on potential synaptic mechanisms underlying learning. These mechanisms have directly driven the careful hand design of biologically plausible models of learning and memory in computational neuroscience [1]. However, these hand designed rules have yet to achieve satisfying success training large neural networks, and are dramatically outperformed by biologically implausible approaches such as backprop. We propose an alternative paradigm for designing biologically plausible learning rules: using meta-learning to learn a parametric synaptic update rule which is capable of training deep networks. We demonstrate this approach by meta-learning an update rule for semi-supervised tasks, where sparse labels are provided to a deep network but the majority of inputs are unlabeled. The meta-learned plasticity rule integrates bottom-up, top-down, and recurrent inputs to each neuron, and generates weight updates as the product of pre- and post- synaptic neuronal outputs. The way in which the inputs to each neuron are combined to produce a learning signal, however, is itself a meta-learned function, parameterized by a neural network. Critically, the meta-learned update rule integrates only neuron-local information when proposing updates–that is, our learning rule is spatially localized to individual neurons. After meta-learning, the resulting synaptic update rule is capable of driving task-relevant learning for semi-supervised tasks. We demonstrate this capability on two simple classification problems. In general, we believe meta-learning to be a powerful approach to finding more effective synaptic plasticity rules, which will motivate new hypotheses for biological neural networks, and new algorithms for artificial neural networks.