Evidence that recurrent circuits are critical to the ventral stream's execution of core object recognition behavior.

Non-recurrent deep convolutional neural networks (CNNs) are currently the best at modeling core object recognition, a behavior that is supported by the densely recurrent primate ventral stream, culminating in the inferior temporal (IT) cortex. If recurrence is critical to this behavior, then primates should outperform feedforward-only deep CNNs for images that require additional recurrent processing beyond the feedforward IT response. Here we first used behavioral methods to discover hundreds of these 'challenge' images. Second, using large-scale electrophysiology, we observed that behaviorally sufficient object identity solutions emerged ~30 ms later in the IT cortex for challenge images compared with primate performance-matched 'control' images. Third, these behaviorally critical late-phase IT response patterns were poorly predicted by feedforward deep CNN activations. Notably, very-deep CNNs and shallower recurrent CNNs better predicted these late IT responses, suggesting that there is a functional equivalence between additional nonlinear transformations and recurrence. Beyond arguing that recurrent circuits are critical for rapid object identification, our results provide strong constraints for future recurrent model development.

Large-Scale, High-Resolution Comparison of the Core Visual Object Recognition Behavior of Humans, Monkeys, and State-of-the-Art Deep Artificial Neural Networks.

Primates, including humans, can typically recognize objects in visual images at a glance despite naturally occurring identity-preserving image transformations (e.g., changes in viewpoint). A primary neuroscience goal is to uncover neuron-level mechanistic models that quantitatively explain this behavior by predicting primate performance for each and every image. Here, we applied this stringent behavioral prediction test to the leading mechanistic models of primate vision (specifically, deep, convolutional, artificial neural networks; ANNs) by directly comparing their behavioral signatures against those of humans and rhesus macaque monkeys. Using high-throughput data collection systems for human and monkey psychophysics, we collected more than one million behavioral trials from 1472 anonymous humans and five male macaque monkeys for 2400 images over 276 binary object discrimination tasks. Consistent with previous work, we observed that state-of-the-art deep, feedforward convolutional ANNs trained for visual categorization (termed DCNNIC models) accurately predicted primate patterns of object-level confusion. However, when we examined behavioral performance for individual images within each object discrimination task, we found that all tested DCNNIC models were significantly nonpredictive of primate performance and that this prediction failure was not accounted for by simple image attributes nor rescued by simple model modifications. These results show that current DCNNIC models cannot account for the image-level behavioral patterns of primates and that new ANN models are needed to more precisely capture the neural mechanisms underlying primate object vision. To this end, large-scale, high-resolution primate behavioral benchmarks such as those obtained here could serve as direct guides for discovering such models.SIGNIFICANCE STATEMENT Recently, specific feedforward deep convolutional artificial neural networks (ANNs) models have dramatically advanced our quantitative understanding of the neural mechanisms underlying primate core object recognition. In this work, we tested the limits of those ANNs by systematically comparing the behavioral responses of these models with the behavioral responses of humans and monkeys at the resolution of individual images. Using these high-resolution metrics, we found that all tested ANN models significantly diverged from primate behavior. Going forward, these high-resolution, large-scale primate behavioral benchmarks could serve as direct guides for discovering better ANN models of the primate visual system.

Comparison of Object Recognition Behavior in Human and Monkey.

Although the rhesus monkey is used widely as an animal model of human visual processing, it is not known whether invariant visual object recognition behavior is quantitatively comparable across monkeys and humans. To address this question, we systematically compared the core object recognition behavior of two monkeys with that of human subjects. To test true object recognition behavior (rather than image matching), we generated several thousand naturalistic synthetic images of 24 basic-level objects with high variation in viewing parameters and image background. Monkeys were trained to perform binary object recognition tasks on a match-to-sample paradigm. Data from 605 human subjects performing the same tasks on Mechanical Turk were aggregated to characterize "pooled human" object recognition behavior, as well as 33 separate Mechanical Turk subjects to characterize individual human subject behavior. Our results show that monkeys learn each new object in a few days, after which they not only match mean human performance but show a pattern of object confusion that is highly correlated with pooled human confusion patterns and is statistically indistinguishable from individual human subjects. Importantly, this shared human and monkey pattern of 3D object confusion is not shared with low-level visual representations (pixels, V1+; models of the retina and primary visual cortex) but is shared with a state-of-the-art computer vision feature representation. Together, these results are consistent with the hypothesis that rhesus monkeys and humans share a common neural shape representation that directly supports object perception. SIGNIFICANCE STATEMENT: To date, several mammalian species have shown promise as animal models for studying the neural mechanisms underlying high-level visual processing in humans. In light of this diversity, making tight comparisons between nonhuman and human primates is particularly critical in determining the best use of nonhuman primates to further the goal of the field of translating knowledge gained from animal models to humans. To the best of our knowledge, this study is the first systematic attempt at comparing a high-level visual behavior of humans and macaque monkeys.