ABSTRACT
Studies of the mouse visual system have revealed a variety of visual brain areas that are thought to support a multitude of behavioral capacities, ranging from stimulus-reward associations, to goal-directed navigation, and object-centric discriminations. However, an overall understanding of the mouse's visual cortex, and how it supports a range of behaviors, remains unknown. Here, we take a computational approach to help address these questions, providing a high-fidelity quantitative model of mouse visual cortex and identifying key structural and functional principles underlying that model's success. Structurally, we find that a comparatively shallow network structure with a low-resolution input is optimal for modeling mouse visual cortex. Our main finding is functional-that models trained with task-agnostic, self-supervised objective functions based on the concept of contrastive embeddings are much better matches to mouse cortex, than models trained on supervised objectives or alternative self-supervised methods. This result is very much unlike in primates where prior work showed that the two were roughly equivalent, naturally leading us to ask the question of why these self-supervised objectives are better matches than supervised ones in mouse. To this end, we show that the self-supervised, contrastive objective builds a general-purpose visual representation that enables the system to achieve better transfer on out-of-distribution visual scene understanding and reward-based navigation tasks. Our results suggest that mouse visual cortex is a low-resolution, shallow network that makes best use of the mouse's limited resources to create a light-weight, general-purpose visual system-in contrast to the deep, high-resolution, and more categorization-dominated visual system of primates.
Subject(s)
Learning , Visual Cortex , Animals , Mice , Brain , Brain Mapping , PrimatesABSTRACT
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.
Subject(s)
Nerve Net/physiology , Neural Networks, Computer , Neurons/physiology , Pattern Recognition, Visual/physiology , Visual Cortex/physiology , Animals , Child , Datasets as Topic , Humans , Macaca/physiology , Nerve Net/anatomy & histology , Unsupervised Machine Learning , Visual Cortex/anatomy & histologyABSTRACT
In this work, we explore the limiting dynamics of deep neural networks trained with stochastic gradient descent (SGD). As observed previously, long after performance has converged, networks continue to move through parameter space by a process of anomalous diffusion in which distance traveled grows as a power law in the number of gradient updates with a nontrivial exponent. We reveal an intricate interaction among the hyperparameters of optimization, the structure in the gradient noise, and the Hessian matrix at the end of training that explains this anomalous diffusion. To build this understanding, we first derive a continuous-time model for SGD with finite learning rates and batch sizes as an underdamped Langevin equation. We study this equation in the setting of linear regression, where we can derive exact, analytic expressions for the phase-space dynamics of the parameters and their instantaneous velocities from initialization to stationarity. Using the Fokker-Planck equation, we show that the key ingredient driving these dynamics is not the original training loss but rather the combination of a modified loss, which implicitly regularizes the velocity, and probability currents that cause oscillations in phase space. We identify qualitative and quantitative predictions of this theory in the dynamics of a ResNet-18 model trained on ImageNet. Through the lens of statistical physics, we uncover a mechanistic origin for the anomalous limiting dynamics of deep neural networks trained with SGD. Understanding the limiting dynamics of SGD, and its dependence on various important hyperparameters like batch size, learning rate, and momentum, can serve as a basis for future work that can turn these insights into algorithmic gains.
ABSTRACT
In the target article, Bowers et al. dispute deep artificial neural network (ANN) models as the currently leading models of human vision without producing alternatives. They eschew the use of public benchmarking platforms to compare vision models with the brain and behavior, and they advocate for a fragmented, phenomenon-specific modeling approach. These are unconstructive to scientific progress. We outline how the Brain-Score community is moving forward to add new model-to-human comparisons to its community-transparent suite of benchmarks.
Subject(s)
Brain , Neural Networks, Computer , HumansABSTRACT
Head-mounted cameras have been used in developmental psychology research for more than a decade to provide a rich and comprehensive view of what infants see during their everyday experiences. However, variation between these devices has limited the field's ability to compare results across studies and across labs. Further, the video data captured by these cameras to date has been relatively low-resolution, limiting how well machine learning algorithms can operate over these rich video data. Here, we provide a well-tested and easily constructed design for a head-mounted camera assembly-the BabyView-developed in collaboration with Daylight Design, LLC., a professional product design firm. The BabyView collects high-resolution video, accelerometer, and gyroscope data from children approximately 6-30 months of age via a GoPro camera custom mounted on a soft child-safety helmet. The BabyView also captures a large, portrait-oriented vertical field-of-view that encompasses both children's interactions with objects and with their social partners. We detail our protocols for video data management and for handling sensitive data from home environments. We also provide customizable materials for onboarding families with the BabyView. We hope that these materials will encourage the wide adoption of the BabyView, allowing the field to collect high-resolution data that can link children's everyday environments with their learning outcomes.
ABSTRACT
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.
Subject(s)
Task Performance and Analysis , Visual Perception , Animals , Humans , Macaca mulatta/physiology , Neural Networks, Computer , Pattern Recognition, Visual/physiology , Recognition, Psychology/physiology , Visual Pathways/physiology , Visual Perception/physiologyABSTRACT
Drawing is a powerful tool that can be used to convey rich perceptual information about objects in the world. What are the neural mechanisms that enable us to produce a recognizable drawing of an object, and how does this visual production experience influence how this object is represented in the brain? Here we evaluate the hypothesis that producing and recognizing an object recruit a shared neural representation, such that repeatedly drawing the object can enhance its perceptual discriminability in the brain. We scanned human participants (N = 31; 11 male) using fMRI across three phases of a training study: during training, participants repeatedly drew two objects in an alternating sequence on an MR-compatible tablet; before and after training, they viewed these and two other control objects, allowing us to measure the neural representation of each object in visual cortex. We found that: (1) stimulus-evoked representations of objects in visual cortex are recruited during visually cued production of drawings of these objects, even throughout the period when the object cue is no longer present; (2) the object currently being drawn is prioritized in visual cortex during drawing production, while other repeatedly drawn objects are suppressed; and (3) patterns of connectivity between regions in occipital and parietal cortex supported enhanced decoding of the currently drawn object across the training phase, suggesting a potential neural substrate for learning how to transform perceptual representations into representational actions. Together, our study provides novel insight into the functional relationship between visual production and recognition in the brain.SIGNIFICANCE STATEMENT Humans can produce simple line drawings that capture rich information about their perceptual experiences. However, the mechanisms that support this behavior are not well understood. Here we investigate how regions in visual cortex participate in the recognition of an object and the production of a drawing of it. We find that these regions carry diagnostic information about an object in a similar format both during recognition and production, and that practice drawing an object enhances transmission of information about it to downstream regions. Together, our study provides novel insight into the functional relationship between visual production and recognition in the brain.
Subject(s)
Pattern Recognition, Visual/physiology , Recognition, Psychology/physiology , Visual Cortex/diagnostic imaging , Adult , Female , Humans , Magnetic Resonance Imaging , Male , Photic Stimulation , Visual Cortex/physiology , Young AdultABSTRACT
The ventral visual stream underlies key human visual object recognition abilities. However, neural encoding in the higher areas of the ventral stream remains poorly understood. Here, we describe a modeling approach that yields a quantitatively accurate model of inferior temporal (IT) cortex, the highest ventral cortical area. Using high-throughput computational techniques, we discovered that, within a class of biologically plausible hierarchical neural network models, there is a strong correlation between a model's categorization performance and its ability to predict individual IT neural unit response data. To pursue this idea, we then identified a high-performing neural network that matches human performance on a range of recognition tasks. Critically, even though we did not constrain this model to match neural data, its top output layer turns out to be highly predictive of IT spiking responses to complex naturalistic images at both the single site and population levels. Moreover, the model's intermediate layers are highly predictive of neural responses in the V4 cortex, a midlevel visual area that provides the dominant cortical input to IT. These results show that performance optimization--applied in a biologically appropriate model class--can be used to build quantitative predictive models of neural processing.
Subject(s)
Macaca mulatta/physiology , Models, Neurological , Neural Networks, Computer , Visual Cortex/physiology , Algorithms , Animals , Humans , Nerve Net/physiology , Photic Stimulation/methods , Psychomotor Performance/physiology , Recognition, Psychology/physiology , Visual Pathways/physiology , Visual Perception/physiologyABSTRACT
Humans can learn to recognize new objects just from observing example views. However, it is unknown what structural information enables this learning. To address this question, we manipulated the amount of structural information given to subjects during unsupervised learning by varying the format of the trained views. We then tested how format affected participants' ability to discriminate similar objects across views that were rotated 90° apart. We found that, after training, participants' performance increased and generalized to new views in the same format. Surprisingly, the improvement was similar across line drawings, shape from shading, and shape from shading + stereo even though the latter two formats provide richer depth information compared to line drawings. In contrast, participants' improvement was significantly lower when training used silhouettes, suggesting that silhouettes do not have enough information to generate a robust 3-D structure. To test whether the learned object representations were format-specific or format-invariant, we examined if learning novel objects from example views transfers across formats. We found that learning objects from example line drawings transferred to shape from shading and vice versa. These results have important implications for theories of object recognition because they suggest that (a) learning the 3-D structure of objects does not require rich structural cues during training as long as shape information of internal and external features is provided and (b) learning generates shape-based object representations independent of the training format.
Subject(s)
Cues , Depth Perception/physiology , Form Perception/physiology , Imaging, Three-Dimensional , Learning , Pattern Recognition, Visual/physiology , Adult , Female , Humans , MaleABSTRACT
The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of "kernel analysis" that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio-inspired models, that possibility cannot be ruled out merely on representational performance grounds.
Subject(s)
Models, Neurological , Nerve Net/physiology , Neural Networks, Computer , Pattern Recognition, Visual/physiology , Temporal Lobe/physiology , Algorithms , Animals , Macaca mulatta , MaleABSTRACT
The Plasmodium falciparum parasite's ability to adapt to environmental pressures, such as the human immune system and antimalarial drugs, makes malaria an enduring burden to public health. Understanding the genetic basis of these adaptations is critical to intervening successfully against malaria. To that end, we created a high-density genotyping array that assays over 17,000 single nucleotide polymorphisms (â¼ 1 SNP/kb), and applied it to 57 culture-adapted parasites from three continents. We characterized genome-wide genetic diversity within and between populations and identified numerous loci with signals of natural selection, suggesting their role in recent adaptation. In addition, we performed a genome-wide association study (GWAS), searching for loci correlated with resistance to thirteen antimalarials; we detected both known and novel resistance loci, including a new halofantrine resistance locus, PF10_0355. Through functional testing we demonstrated that PF10_0355 overexpression decreases sensitivity to halofantrine, mefloquine, and lumefantrine, but not to structurally unrelated antimalarials, and that increased gene copy number mediates resistance. Our GWAS and follow-on functional validation demonstrate the potential of genome-wide studies to elucidate functionally important loci in the malaria parasite genome.
Subject(s)
Antimalarials/pharmacology , Drug Resistance/genetics , Genetic Loci , Plasmodium falciparum/genetics , Ethanolamines/pharmacology , Fluorenes/pharmacology , Gene Dosage , Gene Expression , Genetic Association Studies , Genetic Variation , Genotype , Haplotypes , Linkage Disequilibrium , Lumefantrine , Malaria, Falciparum/parasitology , Malaria, Falciparum/prevention & control , Mefloquine/pharmacology , Phenanthrenes/pharmacology , Plasmodium falciparum/drug effects , Polymorphism, Single Nucleotide , Selection, GeneticABSTRACT
A key feature of cortical systems is functional organization: the arrangement of functionally distinct neurons in characteristic spatial patterns. However, the principles underlying the emergence of functional organization in the cortex are poorly understood. Here, we develop the topographic deep artificial neural network (TDANN), the first model to predict several aspects of the functional organization of multiple cortical areas in the primate visual system. We analyze the factors driving the TDANN's success and find that it balances two objectives: learning a task-general sensory representation and maximizing the spatial smoothness of responses according to a metric that scales with cortical surface area. In turn, the representations learned by the TDANN are more brain-like than in spatially unconstrained models. Finally, we provide evidence that the TDANN's functional organization balances performance with between-area connection length. Our results offer a unified principle for understanding the functional organization of the primate ventral visual system.
Subject(s)
Neural Networks, Computer , Visual Cortex , Visual Cortex/physiology , Animals , Models, Neurological , Visual Pathways/physiology , Neurons/physiologyABSTRACT
A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly understood. Here we develop the Topographic Deep Artificial Neural Network (TDANN), the first unified model to accurately predict the functional organization of multiple cortical areas in the primate visual system. We analyze the key factors responsible for the TDANN's success and find that it strikes a balance between two specific objectives: achieving a task-general sensory representation that is self-supervised, and maximizing the smoothness of responses across the cortical sheet according to a metric that scales relative to cortical surface area. In turn, the representations learned by the TDANN are lower dimensional and more brain-like than those in models that lack a spatial smoothness constraint. Finally, we provide evidence that the TDANN's functional organization balances performance with inter-area connection length, and use the resulting models for a proof-of-principle optimization of cortical prosthetic design. Our results thus offer a unified principle for understanding functional organization and a novel view of the functional role of the visual system in particular.
ABSTRACT
Humans learn from visual inputs at multiple timescales, both rapidly and flexibly acquiring visual knowledge over short periods, and robustly accumulating online learning progress over longer periods. Modeling these powerful learning capabilities is an important problem for computational visual cognitive science, and models that could replicate them would be of substantial utility in real-world computer vision settings. In this work, we establish benchmarks for both real-time and life-long continual visual learning. Our real-time learning benchmark measures a model's ability to match the rapid visual behavior changes of real humans over the course of minutes and hours, given a stream of visual inputs. Our life-long learning benchmark evaluates the performance of models in a purely online learning curriculum obtained directly from child visual experience over the course of years of development. We evaluate a spectrum of recent deep self-supervised visual learning algorithms on both benchmarks, finding that none of them perfectly match human performance, though some algorithms perform substantially better than others. Interestingly, algorithms embodying recent trends in self-supervised learning - including BYOL, SwAV and MAE - are substantially worse on our benchmarks than an earlier generation of self-supervised algorithms such as SimCLR and MoCo-v2. We present analysis indicating that the failure of these newer algorithms is primarily due to their inability to handle the kind of sparse low-diversity datastreams that naturally arise in the real world, and that actively leveraging memory through negative sampling - a mechanism eschewed by these newer algorithms - appears useful for facilitating learning in such low-diversity environments. We also illustrate a complementarity between the short and long timescales in the two benchmarks, showing how requiring a single learning algorithm to be locally context-sensitive enough to match real-time learning changes while stable enough to avoid catastrophic forgetting over the long term induces a trade-off that human-like algorithms may have to straddle. Taken together, our benchmarks establish a quantitative way to directly compare learning between neural networks models and human learners, show how choices in the mechanism by which such algorithms handle sample comparison and memory strongly impact their ability to match human learning abilities, and expose an open problem space for identifying more flexible and robust visual self-supervision algorithms.
ABSTRACT
The medial temporal lobe (MTL) supports a constellation of memory-related behaviors. Its involvement in perceptual processing, however, has been subject to enduring debate. This debate centers on perirhinal cortex (PRC), an MTL structure at the apex of the ventral visual stream (VVS). Here we leverage a deep learning framework that approximates visual behaviors supported by the VVS (i.e., lacking PRC). We first apply this approach retroactively, modeling 30 published visual discrimination experiments: excluding non-diagnostic stimulus sets, there is a striking correspondence between VVS-modeled and PRC-lesioned behavior, while each is outperformed by PRC-intact participants. We corroborate and extend these results with a novel experiment, directly comparing PRC-intact human performance to electrophysiological recordings from the macaque VVS: PRC-intact participants outperform a linear readout of high-level visual cortex. By situating lesion, electrophysiological, and behavioral results within a shared computational framework, this work resolves decades of seemingly inconsistent findings surrounding PRC involvement in perception.
Subject(s)
Models, Neurological , Perirhinal Cortex/physiology , Visual Perception , Animals , Deep Learning , Humans , MacacaABSTRACT
The ventral visual stream is known to be organized hierarchically, where early visual areas processing simplistic features feed into higher visual areas processing more complex features. Hierarchical convolutional neural networks (CNNs) were largely inspired by this type of brain organization and have been successfully used to model neural responses in different areas of the visual system. In this work, we aim to understand how an instance of these models corresponds to temporal dynamics of human object processing. Using representational similarity analysis (RSA) and various similarity metrics, we compare the model representations with two electroencephalography (EEG) data sets containing responses to a shared set of 72 images. We find that there is a hierarchical relationship between the depth of a layer and the time at which peak correlation with the brain response occurs for certain similarity metrics in both data sets. However, when comparing across layers in the neural network, the correlation onset time did not appear in a strictly hierarchical fashion. We present two additional methods that improve upon the achieved correlations by optimally weighting features from the CNN and show that depending on the similarity metric, deeper layers of the CNN provide a better correspondence than shallow layers to later time points in the EEG responses. However, we do not find that shallow layers provide better correspondences than those of deeper layers to early time points, an observation that violates the hierarchy and is in agreement with the finding from the onset-time analysis. This work makes a first comparison of various response features-including multiple similarity metrics and data sets-with respect to a neural network.
Subject(s)
Electroencephalography , Neural Networks, Computer , Visual Cortex/physiology , Visual Perception/physiology , Humans , Signal Processing, Computer-Assisted , Time FactorsABSTRACT
Systems neuroscience seeks explanations for how the brain implements a wide variety of perceptual, cognitive and motor tasks. Conversely, artificial intelligence attempts to design computational systems based on the tasks they will have to solve. In artificial neural networks, the three components specified by design are the objective functions, the learning rules and the architectures. With the growing success of deep learning, which utilizes brain-inspired architectures, these three designed components have increasingly become central to how we model, engineer and optimize complex artificial learning systems. Here we argue that a greater focus on these components would also benefit systems neuroscience. We give examples of how this optimization-based framework can drive theoretical and experimental progress in neuroscience. We contend that this principled perspective on systems neuroscience will help to generate more rapid progress.
Subject(s)
Artificial Intelligence , Deep Learning , Neural Networks, Computer , Animals , Brain/physiology , HumansABSTRACT
Production and comprehension have long been viewed as inseparable components of language. The study of vision, by contrast, has centered almost exclusively on comprehension. Here we investigate drawing-the most basic form of visual production. How do we convey concepts in visual form, and how does refining this skill, in turn, affect recognition? We developed an online platform for collecting large amounts of drawing and recognition data, and applied a deep convolutional neural network model of visual cortex trained only on natural images to explore the hypothesis that drawing recruits the same abstract feature representations that support natural visual object recognition. Consistent with this hypothesis, higher layers of this model captured the abstract features of both drawings and natural images most important for recognition, and people learning to produce more recognizable drawings of objects exhibited enhanced recognition of those objects. These findings could explain why drawing is so effective for communicating visual concepts, they suggest novel approaches for evaluating and refining conceptual knowledge, and they highlight the potential of deep networks for understanding human learning.
Subject(s)
Learning/physiology , Pattern Recognition, Visual/physiology , Recognition, Psychology/physiology , Visual Perception/physiology , Humans , Models, Neurological , Photic StimulationABSTRACT
A core goal of auditory neuroscience is to build quantitative models that predict cortical responses to natural sounds. Reasoning that a complete model of auditory cortex must solve ecologically relevant tasks, we optimized hierarchical neural networks for speech and music recognition. The best-performing network contained separate music and speech pathways following early shared processing, potentially replicating human cortical organization. The network performed both tasks as well as humans and exhibited human-like errors despite not being optimized to do so, suggesting common constraints on network and human performance. The network predicted fMRI voxel responses substantially better than traditional spectrotemporal filter models throughout auditory cortex. It also provided a quantitative signature of cortical representational hierarchy-primary and non-primary responses were best predicted by intermediate and late network layers, respectively. The results suggest that task optimization provides a powerful set of tools for modeling sensory systems.