Computational mechanisms underlying cortical responses to the affordance properties of visual scenes
Authors: Bonner Michael F. , Epstein Russell A. 
Published: August 2017

Biologically inspired deep convolutional neural networks (CNNs), trained for computer vision tasks, have been found to predict cortical responses with remarkable accuracy. However, the complex internal operations of these models remain poorly understood, and the factors that account for their success are unknown. Here we developed a set of techniques for using CNNs to gain insights into the computational mechanisms underlying cortical responses. We focused on responses in the occipital place area (OPA), a scene-selective region of dorsal occipitoparietal cortex. In a previous study, we showed that fMRI activation patterns in the OPA contain information about the navigational affordances of scenes: that is, information about where one can and cannot move within the immediate environment. We hypothesized that this affordance information could be extracted using a set of purely feedforward computations. To test this idea, we examined a deep CNN with a feedforward architecture that had been previously trained for scene classification. We found that the CNN was highly predictive of OPA representations, and, importantly, that it accounted for the portion of OPA variance that reflected the navigational affordances of scenes. The CNN could thus serve as an image-computable candidate model of affordance-related responses in the OPA. We then ran a series ofin silicoexperiments on this model to gain insights into its internal computations. These analyses showed that the computation of affordance-related features relied heavily on visual information at high-spatial frequencies and cardinal orientations, both of which have previously been identified as low-level stimulus preferences of scene-selective visual cortex. These computations also exhibited a strong preference for information in the lower visual field, which is consistent with known retinotopic biases in the OPA. Visualizations of feature selectivity within the CNN suggested that affordance-based responses encoded features that define the layout of the spatial environment, such as boundary-defining junctions and large extended surfaces. Together, these results map the sensory functions of the OPA onto a fully quantitative model that provides insights into its visual computations. More broadly, they advance integrative techniques for understanding visual cortex across multiple level of analysis: from the identification of cortical sensory functions to the modeling of their underlying algorithmic implementations.

AUTHOR SUMMARY

How does visual cortex compute behaviorally relevant properties of the local environment from sensory inputs? For decades, computational models have been able to explain only the earliest stages of biological vision, but recent advances in the engineering of deep neural networks have yielded a breakthrough in the modeling of high-level visual cortex. However, these models are not explicitly designed for testing neurobiological theories, and, like the brain itself, their complex internal operations remain poorly understood. Here we examined a deep neural network for insights into the cortical representation of the navigational affordances of visual scenes. In doing so, we developed a set of high-throughput techniques and statistical tools that are broadly useful for relating the internal operations of neural networks with the information processes of the brain. Our findings demonstrate that a deep neural network with purely feedforward computations can account for the processing of navigational layout in high-level visual cortex. We next performed a series of experiments and visualization analyses on this neural network, which characterized a set of stimulus input features that may be critical for computing navigationally related cortical representations and identified a set of high-level, complex scene features that may serve as a basis set for the cortical coding of navigational layout. These findings suggest a computational mechanism through which high-level visual cortex might encode the spatial structure of the local navigational environment, and they demonstrate an experimental approach for leveraging the power of deep neural networks to understand the visual computations of the brain.