Deep neural networks currently provide the best quantitative models of the response patterns of neurons throughout the primate ventral visual stream. However, such networks have remained implausible as a model of the development of the ventral stream, in part because they are trained with supervised methods requiring many more labels than are accessible to infants during development. Here, we report that recent rapid progress in unsupervised learning has largely closed this gap. We find that neural network models learned with deep unsupervised contrastive embedding methods achieve neural prediction accuracy in multiple ventral visual cortical areas that equals or exceeds that of models derived using today’s best supervised methods and that the mapping of these neural network models’ hidden layers is neuroanatomically consistent across the ventral stream. Strikingly, we find that these methods produce brain-like representations even when trained solely with real human child developmental data collected from head-mounted cameras, despite the fact that these datasets are noisy and limited. We also find that semisupervised deep contrastive embeddings can leverage small numbers of labeled examples to produce representations with substantially improved error-pattern consistency to human behavior. Taken together, these results illustrate a use of unsupervised learning to provide a quantitative model of a multiarea cortical brain system and present a strong candidate for a biologically plausible computational theory of primate sensory learning.

Deep artificial neural networks with spatially repeated processing (a.k.a., deep convolutional ANNs) have been established as the best class of candidate models of visual processing in primate ventral visual processing stream. Over the past five years, these ANNs have evolved from a simple feedforward eight-layer architecture in AlexNet to extremely deep and branching NAS-Net architectures, demonstrating increasingly better object categorization performance and increasingly better explanatory power of both neural and behavioral responses. However, from the neuroscientist's point of view, the relationship between such very deep architectures and the ventral visual pathway is incomplete in at least two ways. On the one hand, current stateof-the-art ANNs appear to be too complex (e.g., now over 100 levels) compared with the relatively shallow cortical hierarchy (4-8 levels), which makes it difficult to map their elements to those in the ventral visual stream and to understand what they are doing. On the other hand, current state-of-the-art ANNs appear to be not complex enough in that they lack recurrent connections and the resulting neural response dynamics that are commonplace in the ventral visual stream. Here we describe our ongoing efforts to resolve both of these issues by developing a "CORnet" family of deep neural network architectures. Rather than just seeking high object recognition performance (as the state-of-the-art ANNs above), we instead try to reduce the model family to its most important elements and then gradually build new ANNs with recurrent and skip connections while monitoring both performance and the match between each new CORnet model and a large body of primate brain and behavioral data. We report here that our current best ANN model derived from this approach (CORnet-S) is among the top models on Brain-Score, a composite benchmark for comparing models to the brain, but is simpler than other deep ANNs in terms of the number of convolutions performed along the longest path of information processing in the model. All CORnet models are available at github.com/dicarlolab/CORnet, and we plan to update this manuscript and the available models in this family as they are produced. object recognition | deep neural networks | feedforward | recurrence Correspondence: qbilius@mit.edu (J.K), mschrimpf@mit.edu (M.S.), dicarlo@mit.edu (J.J.D.) * Equal contribution We do not criticize the machine learning and computer vi-Kubilius, Schrimpf et al. | bioRχiv | September 4, 2018 | 1-9

Deep neural networks currently provide the best quantitative models of the response patterns of neurons throughout the primate ventral visual stream. However, such networks have remained implausible as a model of the development of the ventral stream, in part because they are trained with supervised methods requiring many more labels than are accessible to infants during development. Here, we report that recent rapid progress in unsupervised learning has largely closed this gap. We find that neural network models learned with deep unsupervised contrastive embedding methods achieve neural prediction accuracy in multiple ventral visual cortical areas that equals or exceeds that of models derived using today’s best supervised methods, and that the mapping of these neural network models’ hidden layers is neuroanatomically consistent across the ventral stream. Moreover, we find that these methods produce brain-like representations even when trained on noisy and limited data measured from real children’s developmental experience. We also find that semi-supervised deep contrastive embeddings can leverage small numbers of labelled examples to produce representations with substantially improved error-pattern consistency to human behavior. Taken together, these results suggest that deep contrastive embedding objectives may be a biologically-plausible computational theory of primate visual development.

Medial entorhinal cortex (MEC) supports a wide range of navigational and memory related behaviors. Well-known experimental results have revealed specialized cell types in MEC — e.g. grid, border, and head-direction cells — whose highly stereo-typical response profiles are suggestive of the role they might play in supporting MEC functionality. However, the majority of MEC neurons do not exhibit stereotypical firing patterns. How should the response profiles of these more “heterogeneous” cells be described, and how do they contribute to behavior? In this work, we took a computational approach to addressing these questions. We first performed a statistical analysis that shows that heterogeneous MEC cells are just as reliable in their response patterns as the more stereotypical cell types, suggesting that they have a coherent functional role. Next, we evaluated a spectrum of candidate models in terms of their ability to describe the response profiles of both stereotypical and heterogeneous MEC cells. We found that recently developed task-optimized neural network models are substantially better than traditional grid cell-centric models at matching most MEC neuronal response profiles — including those of grid cells themselves — despite not being explicitly trained for this purpose. Specific choices of network architecture (such as gated nonlinearities and an explicit intermediate place cell representation) have an important effect on the ability of the model to generalize to novel scenarios, with the best of these models closely approaching the noise ceiling of the data itself. We then performed “in-silica” experiments on this model to address questions involving the relative functional relevance of various cell types, finding that heterogeneous cells are likely to be just as involved in downstream functional outcomes (such as path integration) as grid and border cells. Finally, inspired by recent data showing that, going beyond their spatial response selectivity, MEC cells are also responsive to non-spatial rewards, we introduce a new MEC model that performs reward-modulated path integration. We find that this unified model matches neural recordings across all variable-reward conditions. Taken together, our results point toward a conceptually principled goal-driven modeling approach for moving future experimental and computational efforts beyond overly-simplistic single-cell stereotypes.

The normal function of the retina is to convey information about natural visual images. It is this visual environment that has driven evolution, and that is clinically relevant. Yet nearly all of our understanding of the neural computations, biological function, and circuit mechanisms of the retina comes in the context of artificially structured stimuli such as flashing spots, moving bars and white noise. It is fundamentally unclear how these artificial stimuli are related to circuit processes engaged under natural stimuli. A key barrier is the lack of methods for analyzing retinal responses to natural images. We addressed both these issues by applying convolutional neural network models (CNNs) to capture retinal responses to natural scenes. We find that CNN models predict natural scene responses with high accuracy, achieving performance close to the fundamental limits of predictability set by intrinsic cellular variability. Furthermore, individual internal units of the model are highly correlated with actual retinal interneuron responses that were recorded separately and never presented to the model during training. Finally, we find that models fit only to natural scenes, but not white noise, reproduce a range of phenomena previously described using distinct artificial stimuli, including frequency doubling, latency encoding, motion anticipation, fast contrast adaptation, synchronized responses to motion reversal and object motion sensitivity. Further examination of the model revealed extremely rapid context dependence of retinal feature sensitivity under natural scenes using an analysis not feasible from direct examination of retinal responses. Overall, these results show that nonlinear retinal processes engaged by artificial stimuli are also engaged in and relevant to natural visual processing, and that CNN models form a powerful and unifying tool to study how sensory circuitry produces computations in a natural context.

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The computational role of the abundant feedback connections in the ventral visual stream is unclear, enabling humans and nonhuman primates to effortlessly recognize objects across a multitude of viewing conditions. Prior studies have augmented feedforward convolutional neural networks (CNNs) with recurrent connections to study their role in visual processing; however, often these recurrent networks are optimized directly on neural data or the comparative metrics used are undefined for standard feedforward networks that lack these connections. In this work, we develop task-optimized convolutional recurrent (ConvRNN) network models that more correctly mimic the timing and gross neuroanatomy of the ventral pathway. Properly chosen intermediate-depth ConvRNN circuit architectures, which incorporate mechanisms of feedforward bypassing and recurrent gating, can achieve high performance on a core recognition task, comparable to that of much deeper feedforward networks. We then develop methods that allow us to compare both CNNs and ConvRNNs to finely grained measurements of primate categorization behavior and neural response trajectories across thousands of stimuli. We find that high-performing ConvRNNs provide a better match to these data than feedforward networks of any depth, predicting the precise timings at which each stimulus is behaviorally decoded from neural activation patterns. Moreover, these ConvRNN circuits consistently produce quantitatively accurate predictions of neural dynamics from V4 and IT across the entire stimulus presentation. In fact, we find that the highest-performing ConvRNNs, which best match neural and behavioral data, also achieve a strong Pareto trade-off between task performance and overall network size. Taken together, our results suggest the functional purpose of recurrence in the ventral pathway is to fit a high-performing network in cortex, attaining computational power through temporal rather than spatial complexity.