A Goal-Driven Approach to Systems Neuroscience

Humans and animals exhibit a range of interesting behaviors in dynamic environments, and it is unclear how our brains actively reformat this dense sensory information to enable these behaviors. Experimental neuroscience is undergoing a revolution in its ability to record and manipulate hundreds to thousands of neurons while an animal is performing a complex behavior. As these paradigms enable unprecedented access to the brain, a natural question that arises is how to distill these data into interpretable insights about how neural circuits give rise to intelligent behaviors. The classical approach in systems neuroscience has been to ascribe well-defined operations to individual neurons and provide a description of how these operations combine to produce a circuit-level theory of neural computations. While this approach has had some success for small-scale recordings with simple stimuli, designed to probe a particular circuit computation, often times these ultimately lead to disparate descriptions of the same system across stimuli. Perhaps more strikingly, many response profiles of neurons are difficult to succinctly describe in words, suggesting that new approaches are needed in light of these experimental observations. In this thesis, we offer a different definition of interpretability that we show has promise in yielding unified structural and functional models of neural circuits, and describes the evolutionary constraints that give rise to the response properties of the neural population, including those that have previously been difficult to describe individually. We demonstrate the utility of this framework across multiple brain areas and species to study the roles of recurrent processing in the primate ventral visual pathway; mouse visual processing; heterogeneity in rodent medial entorhinal cortex; and facilitating biological learning.

Neural Foundations of Mental Simulation: Future Prediction of Latent Representations on Dynamic Scenes

Humans and animals have a rich and flexible understanding of the physical world, which enables them to infer the underlying dynamical trajectories of objects and events, plausible future states, and use that to plan and anticipate the consequences of actions. However, the neural mechanisms underlying these computations are unclear. We combine a goal-driven modeling approach with dense neurophysiological data and high-throughput human behavioral readouts to directly impinge on this question. Specifically, we construct and evaluate several classes of sensory-cognitive networks to predict the future state of rich, ethologically-relevant environments, ranging from self-supervised end-to-end models with pixel-wise or object-centric objectives, to models that future predict in the latent space of purely static image-based or dynamic video-based pretrained foundation models. We find strong differentiation across these model classes in their ability to predict neural and behavioral data both within and across diverse environments. In particular, we find that neural responses are currently best predicted by models trained to predict the future state of their environment in the latent space of pretrained foundation models optimized for dynamic scenes in a self-supervised manner. Notably, models that future predict in the latent space of video foundation models that are optimized to support a diverse range of sensorimotor tasks, reasonably match both human behavioral error patterns and neural dynamics across all environmental scenarios that we were able to test. Overall, these findings suggest that the neural mechanisms and behaviors of primate mental simulation are thus far most consistent with being optimized to future predict on dynamic, reusable visual representations that are useful for embodied AI more generally.

Identifying Learning Rules From Neural Network Observables

The brain modifies its synaptic strengths during learning in order to better adapt to its environment. However, the underlying plasticity rules that govern learning are unknown. Many proposals have been suggested, including Hebbian mechanisms, explicit error backpropagation, and a variety of alternatives. It is an open question as to what specific experimental measurements would need to be made to determine whether any given learning rule is operative in a real biological system. In this work, we take a "virtual experimental" approach to this problem. Simulating idealized neuroscience experiments with artificial neural networks, we generate a large-scale dataset of learning trajectories of aggregate statistics measured in a variety of neural network architectures, loss functions, learning rule hyperparameters, and parameter initializations. We then take a discriminative approach, training linear and simple non-linear classifiers to identify learning rules from features based on these observables. We show that different classes of learning rules can be separated solely on the basis of aggregate statistics of the weights, activations, or instantaneous layer-wise activity changes, and that these results generalize to limited access to the trajectory and held-out architectures and learning curricula. We identify the statistics of each observable that are most relevant for rule identification, finding that statistics from network activities across training are more robust to unit undersampling and measurement noise than those obtained from the synaptic strengths. Our results suggest that activation patterns, available from electrophysiological recordings of post-synaptic activities on the order of several hundred units, frequently measured at wider intervals over the course of learning, may provide a good basis on which to identify learning rules.

Learning Physical Graph Representations from Visual Scenes

Convolutional Neural Networks (CNNs) have proved exceptional at learning representations for visual object categorization. However, CNNs do not explicitly encode objects, parts, and their physical properties, which has limited CNNs' success on tasks that require structured understanding of visual scenes. To overcome these limitations, we introduce the idea of Physical Scene Graphs (PSGs), which represent scenes as hierarchical graphs, with nodes in the hierarchy corresponding intuitively to object parts at different scales, and edges to physical connections between parts. Bound to each node is a vector of latent attributes that intuitively represent object properties such as surface shape and texture. We also describe PSGNet, a network architecture that learns to extract PSGs by reconstructing scenes through a PSG-structured bottleneck. PSGNet augments standard CNNs by including: recurrent feedback connections to combine low and high-level image information; graph pooling and vectorization operations that convert spatially-uniform feature maps into object-centric graph structures; and perceptual grouping principles to encourage the identification of meaningful scene elements. We show that PSGNet outperforms alternative self-supervised scene representation algorithms at scene segmentation tasks, especially on complex real-world images, and generalizes well to unseen object types and scene arrangements. PSGNet is also able learn from physical motion, enhancing scene estimates even for static images. We present a series of ablation studies illustrating the importance of each component of the PSGNet architecture, analyses showing that learned latent attributes capture intuitive scene properties, and illustrate the use of PSGs for compositional scene inference.

Two Routes to Scalable Credit Assignment without Weight Symmetry

The neural plausibility of backpropagation has long been disputed, primarily for its use of non-local weight transport - the biologically dubious requirement that one neuron instantaneously measure the synaptic weights of another. Until recently, attempts to create local learning rules that avoid weight transport have typically failed in the large-scale learning scenarios where backpropagation shines, e.g. ImageNet categorization with deep convolutional networks. Here, we investigate a recently proposed local learning rule that yields competitive performance with backpropagation and find that it is highly sensitive to metaparameter choices, requiring laborious tuning that does not transfer across network architecture. Our analysis indicates the underlying mathematical reason for this instability, allowing us to identify a more robust local learning rule that better transfers without metaparameter tuning. Nonetheless, we find a performance and stability gap between this local rule and backpropagation that widens with increasing model depth. We then investigate several non-local learning rules that relax the need for instantaneous weight transport into a more biologically-plausible "weight estimation" process, showing that these rules match state-of-the-art performance on deep networks and operate effectively in the presence of noisy updates. Taken together, our results suggest two routes towards the discovery of neural implementations for credit assignment without weight symmetry: further improvement of local rules so that they perform consistently across architectures and the identification of biological implementations for non-local learning mechanisms.

From deep learning to mechanistic understanding in neuroscience: the structure of retinal prediction

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.

Brain-Like Object Recognition with High-Performing Shallow Recurrent ANNs

Deep convolutional artificial neural networks (ANNs) are the leading class of candidate models of the mechanisms of visual processing in the primate ventral stream. While initially inspired by brain anatomy, over the past years, these ANNs have evolved from a simple eight-layer architecture in AlexNet to extremely deep and branching architectures, demonstrating increasingly better object categorization performance, yet bringing into question how brain-like they still are. In particular, typical deep models from the machine learning community are often hard to map onto the brain's anatomy due to their vast number of layers and missing biologically-important connections, such as recurrence. Here we demonstrate that better anatomical alignment to the brain and high performance on machine learning as well as neuroscience measures do not have to be in contradiction. We developed CORnet-S, a shallow ANN with four anatomically mapped areas and recurrent connectivity, guided by Brain-Score, a new large-scale composite of neural and behavioral benchmarks for quantifying the functional fidelity of models of the primate ventral visual stream. Despite being significantly shallower than most models, CORnet-S is the top model on Brain-Score and outperforms similarly compact models on ImageNet. Moreover, our extensive analyses of CORnet-S circuitry variants reveal that recurrence is the main predictive factor of both Brain-Score and ImageNet top-1 performance. Finally, we report that the temporal evolution of the CORnet-S "IT" neural population resembles the actual monkey IT population dynamics. Taken together, these results establish CORnet-S, a compact, recurrent ANN, as the current best model of the primate ventral visual stream.

Task-Driven Convolutional Recurrent Models of the Visual System

Feed-forward convolutional neural networks (CNNs) are currently state-of-the-art for object classification tasks such as ImageNet. Further, they are quantitatively accurate models of temporally-averaged responses of neurons in the primate brain's visual system. However, biological visual systems have two ubiquitous architectural features not shared with typical CNNs: local recurrence within cortical areas, and long-range feedback from downstream areas to upstream areas. Here we explored the role of recurrence in improving classification performance. We found that standard forms of recurrence (vanilla RNNs and LSTMs) do not perform well within deep CNNs on the ImageNet task. In contrast, novel cells that incorporated two structural features, bypassing and gating, were able to boost task accuracy substantially. We extended these design principles in an automated search over thousands of model architectures, which identified novel local recurrent cells and long-range feedback connections useful for object recognition. Moreover, these task-optimized ConvRNNs matched the dynamics of neural activity in the primate visual system better than feedforward networks, suggesting a role for the brain's recurrent connections in performing difficult visual behaviors.

Biologically inspired protection of deep networks from adversarial attacks

Inspired by biophysical principles underlying nonlinear dendritic computation in neural circuits, we develop a scheme to train deep neural networks to make them robust to adversarial attacks. Our scheme generates highly nonlinear, saturated neural networks that achieve state of the art performance on gradient based adversarial examples on MNIST, despite never being exposed to adversarially chosen examples during training. Moreover, these networks exhibit unprecedented robustness to targeted, iterative schemes for generating adversarial examples, including second-order methods. We further identify principles governing how these networks achieve their robustness, drawing on methods from information geometry. We find these networks progressively create highly flat and compressed internal representations that are sensitive to very few input dimensions, while still solving the task. Moreover, they employ highly kurtotic weight distributions, also found in the brain, and we demonstrate how such kurtosis can protect even linear classifiers from adversarial attack.

Deep Learning Models of the Retinal Response to Natural Scenes

A central challenge in neuroscience is to understand neural computations and circuit mechanisms that underlie the encoding of ethologically relevant, natural stimuli. In multilayered neural circuits, nonlinear processes such as synaptic transmission and spiking dynamics present a significant obstacle to the creation of accurate computational models of responses to natural stimuli. Here we demonstrate that deep convolutional neural networks (CNNs) capture retinal responses to natural scenes nearly to within the variability of a cell's response, and are markedly more accurate than linear-nonlinear (LN) models and Generalized Linear Models (GLMs). Moreover, we find two additional surprising properties of CNNs: they are less susceptible to overfitting than their LN counterparts when trained on small amounts of data, and generalize better when tested on stimuli drawn from a different distribution (e.g. between natural scenes and white noise). Examination of trained CNNs reveals several properties. First, a richer set of feature maps is necessary for predicting the responses to natural scenes compared to white noise. Second, temporally precise responses to slowly varying inputs originate from feedforward inhibition, similar to known retinal mechanisms. Third, the injection of latent noise sources in intermediate layers enables our model to capture the sub-Poisson spiking variability observed in retinal ganglion cells. Fourth, augmenting our CNNs with recurrent lateral connections enables them to capture contrast adaptation as an emergent property of accurately describing retinal responses to natural scenes. These methods can be readily generalized to other sensory modalities and stimulus ensembles. Overall, this work demonstrates that CNNs not only accurately capture sensory circuit responses to natural scenes, but also yield information about the circuit's internal structure and function.