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Epstein, R. A.

Publications and source records attributed to Epstein, R. A..

7 recordsLinked to original sources

Cognitive maps for hierarchical spaces in the human brain

Many of the environments that we navigate through every day are hierarchically organized--they consist of spaces nested within other spaces. How do our mind/brains represent such environments? To address this question, we familiarized participants with a virtual environment consisting of a building within a courtyard, with objects distributed throughout the courtyard and building interior. We then scanned them with fMRI while they performed a memory task that required them to think about spatial relationships within and across the subspaces. Behavioral responses were less accurate and response times were longer on trials requiring integration across the subspaces compared to trials not requiring integration. fMRI response differences between integration and non-integration trials were observed in scene-responsive and medial temporal lobe brain regions, which were correlated the behavioral integration effects in retrosplenial complex, occipital place area, and hippocampus. Multivoxel pattern analyses provided additional evidence for representations in these brain regions that reflected the hierarchical organization of the environment. These results indicate that people form cognitive maps of nested spaces by dividing them into subspaces and using an active cognitive process to integrate the subspaces. Similar mechanisms might be used to support hierarchical coding in memory more broadly.

neuroscience↗

Distinct mechanisms for panoramic and landmark-based view integration in human scene-selective cortex

To encode a cognitive map of an environment, a navigating agent must be able to integrate across disparate perceptual views corresponding to the same place. There are two ways that this can be done. First, the agent might integrate across the panorama of views obtainable at a single vantage point. Second, they might integrate across views of a distal location containing a landmark that is visible from multiple vantage points. Guided by previous work, we tested the hypothesis that these two viewpoint-integration processes would be mediated by different neuroanatomical substrates. Male and female human participants were familiarized with a route through a virtual city, along which they closely viewed 24 storefronts that were pairwise associated, either by being located on different buildings directly across the street from each other (same-panorama condition) or by being located on different sides of the same building facing different streets (same-landmark condition). They were then scanned with fMRI while viewing the storefronts in isolation and performing a spatial memory task. Multivoxel pattern analysis revealed a functional distinction between two scene-selective regions: the retrosplenial complex (RSC) showed a significant association effect for same-panorama storefronts, whereas the parahippocampal place area (PPA) showed a significant association effect for same-landmark storefronts. Panoramic association effects were also observed in several other dorsal-stream regions within the medial and lateral parietal lobe. These results demonstrate the existence of two neural mechanisms for integrating across views to represent places as either the observers location (same panorama) or the observed location (same landmark). SIGNIFICANCE STATEMENTAn important component of spatial navigation is the ability to integrate across disparate views corresponding to the same place. Here we tested the idea that there are two such integration mechanisms in the human brain. Participants were familiarized with a virtual city and then scanned with fMRI while viewing storefronts from that city. Using multivariate pattern analysis, we find that the retrosplenial complex (RSC) and other parietal regions encode panoramas of views observed from specific locations, whereas the parahippocampal place area (PPA) encodes sets of views corresponding to specific landmarks. These results reveal two anatomically separated mechanisms for integrating views into places, thus advancing our understanding of how the brain forms cognitive maps of spatial environments.

neuroscience↗

Neural compass in the human brain during naturalistic virtual navigation

A central component of wayfinding is the ability to maintain a consistent representation of ones facing direction when moving about the world. In rodents, head direction cells are believed to support this "neural compass", but identifying a similar mechanism in humans during dynamic naturalistic navigation has been challenging. To address this issue, we acquired fMRI data while participants freely navigated through a virtual reality city. Encoding model analyses revealed voxel clusters in retrosplenial complex and superior parietal lobule that exhibited reliable tuning as a function of facing direction. Crucially, these directional tunings were consistent across perceptually different versions of the city, spatially separated locations within the city, and motivationally distinct phases of the behavioral task. Analysis of the model weights indicated that these regions may represent facing direction relative to the principal axis of the environment. These findings reveal specific mechanisms in the human brain that allow us to maintain a sense of direction during naturalistic, dynamic navigation.

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Object representations in the human brain reflect the co-occurrence statistics of vision and language

A central regularity of visual perception is the co-occurrence of objects in the natural environment. Here we use machine learning and fMRI to test the hypothesis that object co-occurrence statistics are encoded in the human visual system and elicited by the perception of individual objects. We identified low-dimensional representations that capture the latent statistical structure of object co-occurrence in real-world scenes, and we mapped these statistical representations onto voxelwise fMRI responses during object viewing. We found that cortical responses to single objects were predicted by the statistical ensembles in which they typically occur, and that this link between objects and their visual contexts was made most strongly in the anterior portion of the scene-selective parahippocampal place area. In contrast, a language-based statistical model of the co-occurrence of object names in written text predicted responses in neighboring regions of object-selective visual cortex. Together, these findings show that the sensory coding of objects in the human brain reflects the latent statistics of object context in visual and linguistic experience.

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Adaptation decorrelates shape representations

Perception and neural responses are modulated by sensory history. Visual adaptation, an example of such an effect, has been hypothesized to improve stimulus discrimination by decorrelating responses across a set of neural units. While a central theoretical model, behavioral and neural evidence for this theory is limited and inconclusive. Here, we use a parametric 3D shape-space to test whether adaptation decorrelates shape representations in humans. In a behavioral experiment with 20 subjects, we find that adaptation to a shape class improves discrimination of subsequently presented stimuli with similar features. In a BOLD fMRI experiment with 10 subjects we observe that adaptation to a shape class decorrelates the multivariate representations of subsequently presented stimuli with similar features in object-selective cortex. These results support the long-standing proposal that adaptation improves perceptual discrimination and decorrelates neural representations, offering insights into potential underlying mechanisms.

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Computational mechanisms underlying cortical responses to the affordance properties of visual scenes

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 of in silico experiments 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.\n\nAUTHOR SUMMARYHow 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.

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Environmental deformations dynamically shift the spatial metric of the brain

Environmental deformations induce stereotyped distortions in the time-averaged activity of grid and place cells. We hypothesized that these effects are partly driven by border cell inputs which reset the spatial phase of grid cells, maintaining learned relationships between grid phase and environmental boundaries without altering inherent grid scale. A computational model of this mechanism reproduced diverse distortions during deformations, including scale-dependent and local distortions of grid fields, and stretched, duplicated, and fractured place fields. This model predicted a striking new effect: dynamic, history-dependent, boundary-tethered shifts in grid phase during deformations. We reanalyzed two rodent grid cell rescaling datasets and found direct evidence of these shifts, which have not been previously reported and contribute to the appearance of rescaling. These results demonstrate that the grid representation of geometrically deformed environments is not fixed, but rather dynamically changes with the specific experience of the navigator.

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