Ha Hong

Performance-optimized hierarchical models predict neural responses in higher visual cortex

Significance Humans and monkeys easily recognize objects in scenes. This ability is known to be supported by a network of hierarchically interconnected brain areas. However, understanding neurons in higher levels of this hierarchy has long remained a major challenge in visual systems neuroscience. We use computational techniques to identify a neural network model that matches human performance on challenging object categorization tasks. Although not explicitly constrained to match neural data, this model turns out to be highly predictive of neural responses in both the V4 and inferior temporal cortex, the top two layers of the ventral visual hierarchy. In addition to yielding greatly improved models of visual cortex, these results suggest that a process of biological performance optimization directly shaped neural mechanisms. 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.

Deep Neural Networks Rival the Representation of Primate IT Cortex for Core Visual Object Recognition

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.

Simple Learned Weighted Sums of Inferior Temporal Neuronal Firing Rates Accurately Predict Human Core Object Recognition Performance.

To go beyond qualitative models of the biological substrate of object recognition, we ask: can a single ventral stream neuronal linking hypothesis quantitatively account for core object recognition performance over a broad range of tasks? We measured human performance in 64 object recognition tests using thousands of challenging images that explore shape similarity and identity preserving object variation. We then used multielectrode arrays to measure neuronal population responses to those same images in visual areas V4 and inferior temporal (IT) cortex of monkeys and simulated V1 population responses. We tested leading candidate linking hypotheses and control hypotheses, each postulating how ventral stream neuronal responses underlie object recognition behavior. Specifically, for each hypothesis, we computed the predicted performance on the 64 tests and compared it with the measured pattern of human performance. All tested hypotheses based on low- and mid-level visually evoked activity (pixels, V1, and V4) were very poor predictors of the human behavioral pattern. However, simple learned weighted sums of distributed average IT firing rates exactly predicted the behavioral pattern. More elaborate linking hypotheses relying on IT trial-by-trial correlational structure, finer IT temporal codes, or ones that strictly respect the known spatial substructures of IT (“face patches”) did not improve predictive power. Although these results do not reject those more elaborate hypotheses, they suggest a simple, sufficient quantitative model: each object recognition task is learned from the spatially distributed mean firing rates (100 ms) of ∼60,000 IT neurons and is executed as a simple weighted sum of those firing rates. SIGNIFICANCE STATEMENT We sought to go beyond qualitative models of visual object recognition and determine whether a single neuronal linking hypothesis can quantitatively account for core object recognition behavior. To achieve this, we designed a database of images for evaluating object recognition performance. We used multielectrode arrays to characterize hundreds of neurons in the visual ventral stream of nonhuman primates and measured the object recognition performance of >100 human observers. Remarkably, we found that simple learned weighted sums of firing rates of neurons in monkey inferior temporal (IT) cortex accurately predicted human performance. Although previous work led us to expect that IT would outperform V4, we were surprised by the quantitative precision with which simple IT-based linking hypotheses accounted for human behavior.

A performance-optimized model of neural responses across the ventral visual stream

Human visual object recognition is subserved by a multitude of cortical areas. To make sense of this system, one line of research focused on response properties of primary visual cortex neurons and developed theoretical models of a set of canonical computations such as convolution, thresholding, exponentiating and normalization that could be hierarchically repeated to give rise to more complex representations. Another line or research focused on response properties of high-level visual cortex and linked these to semantic categories useful for object recognition. Here, we hypothesized that the panoply of visual representations in the human ventral stream may be understood as emergent properties of a system constrained both by simple canonical computations and by top-level, object recognition functionality in a single unified framework (Yamins et al., 2014; Khaligh-Razavi and Kriegeskorte, 2014; Güçlü and van Gerven, 2015). We built a deep convolutional neural network model optimized for object recognition and compared representations at various model levels using representational similarity analysis to human functional imaging responses elicited from viewing hundreds of image stimuli. Neural network layers developed representations that corresponded in a hierarchical consistent fashion to visual areas from V1 to LOC. This correspondence increased with optimization of the model’s recognition performance. These findings support a unified view of the ventral stream in which representations from the earliest to the latest stages can be understood as being built from basic computations inspired by modeling of early visual cortex shaped by optimization for high-level object-based performance constraints. Significance Statement Prior work has taken two complimentary approaches to understanding the cortical processes underlying our ability to visually recognize objects. One approach identified canonical computations from primary visual cortex that could be hierarchically repeated and give rise to complex representations. Another approach linked later visual area responses to semantic categories useful for object recognition. Here we combined both approaches by optimizing a deep convolution neural network based on canonical computations to preform object recognition. We found that this network developed hierarchically similar response properties to those of visual areas we measured using functional imaging. Thus, we show that object-based performance optimization results in predictive models that not only share similarity with late visual areas, but also intermediate and early visual areas.

Brain-Score: Which Artificial Neural Network for Object Recognition is most Brain-Like?

The internal representations of early deep artificial neural networks (ANNs) were found to be remarkably similar to the internal neural representations measured experimentally in the primate brain. Here we ask, as deep ANNs have continued to evolve, are they becoming more or less brain-like? ANNs that are most functionally similar to the brain will contain mechanisms that are most like those used by the brain. We therefore developed Brain-Score – a composite of multiple neural and behavioral benchmarks that score any ANN on how similar it is to the brain’s mechanisms for core object recognition – and we deployed it to evaluate a wide range of state-of-the-art deep ANNs. Using this scoring system, we here report that: (1) DenseNet-169, CORnet-S and ResNet-101 are the most brain-like ANNs. There remains considerable variability in neural and behavioral responses that is not predicted by any ANN, suggesting that no ANN model has yet captured all the relevant mechanisms. (3) Extending prior work, we found that gains in ANN ImageNet performance led to gains on Brain-Score. However, correlation weakened at ≥ 70% top-1 ImageNet performance, suggesting that additional guidance from neuroscience is needed to make further advances in capturing brain mechanisms. (4) We uncovered smaller (i.e. less complex) ANNs that are more brain-like than many of the best-performing ImageNet models, which suggests the opportunity to simplify ANNs to better understand the ventral stream. The scoring system used here is far from complete. However, we propose that evaluating and tracking model-benchmark correspondences through a Brain-Score that is regularly updated with new brain data is an exciting opportunity: experimental benchmarks can be used to guide machine network evolution, and machine networks are mechanistic hypotheses of the brain’s network and thus drive next experiments. To facilitate both of these, we release Brain-Score.org: a platform that hosts the neural and behavioral benchmarks, where ANNs for visual processing can be submitted to receive a Brain-Score and their rank relative to other models, and where new experimental data can be naturally incorporated.