A fundamental aspect of our existence is the fact that we move through space. We do not do so randomly~ rather, we use a variety of different strategies to efficiently reach our navigational goals. One such strategy is landmark-based piloting, which is the use of stable topological features to determine one's location and orientation relative to the enduring spatial structure of the world. The current proposal describes a research program in which functional magnetic resonance imaging (fMRI) and cognitive behavioral testing are used to understand the neural mechanisms that underlie landmark-based piloting. Previous neuroimaging and neuropsychological studies, including several from our laboratory, have identified a network of brain regions that might be critical. These include the parahippocampal place area (PPA), the retrosplenial complex (RSC), and the hippocampus. However, the precise way in which this network implements this function remains unclear. We will use recent technical innovations for the study of neural representation-multi-voxel pattern analyses (MVPA) and fMRI adaptation (fMRIa) - to test the idea that this network can be fractionated into functional subsystems tied to three cognitive mechanisms: a landmark-recognition mechanism, a spatial orientation mechanism, and a cognitive map. More specifically, Aim 1 will test the hypothesis that the PPA encodes fixed landmarks and local spatial coordinate frames that are anchored to these landmarks.
Aim 2 will test the hypothesis that RSC supports recovery of location and facing direction relative to global (beyond-the-horizon) coordinate frames.
Aim 3 will test the idea that the hippocampus encodes a cognitive map, by characterizing the spatial code indexed by a recently-discovered hippocampal distance signal. If successful, this research will result in a detailed theory of the neural basis of landmak-based piloting. This knowledge will have important health implications in two domains. First, understanding the mechanisms that underlie landmark-based piloting is critical for the development of rehabilitation strategies and navigational aids for the blind. Second, because the brain regions investigated are often impacted early in neurodegenerative diseases such as Alzheimer's dementia, the knowledge gained about these systems will be useful for diagnosing and managing these diseases.

Public Health Relevance

This project examines the neural mechanisms underlying landmark-based spatial navigation. This knowledge is important for developing rehabilitation strategies in people with impaired sight, who often suffer from wayfinding difficulties. Moreover, because the brain regions that support spatial navigation are typically impacted early in neurodegenerative diseases such as Alzheimer's dementia, knowledge about these systems is important for developing strategies for diagnosing and managing these diseases.

National Institute of Health (NIH)
National Eye Institute (NEI)
Research Project (R01)
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Cognition and Perception Study Section (CP)
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Steinmetz, Michael A
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University of Pennsylvania
Schools of Arts and Sciences
United States
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Julian, Joshua B; Kamps, Frederik S; Epstein, Russell A et al. (2018) Dissociable spatial memory systems revealed by typical and atypical human development. Dev Sci :e12737
Julian, Joshua B; Keinath, Alexandra T; Frazzetta, Giulia et al. (2018) Human entorhinal cortex represents visual space using a boundary-anchored grid. Nat Neurosci 21:191-194
Keinath, Alexandra T; Epstein, Russell A; Balasubramanian, Vijay (2018) Environmental deformations dynamically shift the grid cell spatial metric. Elife 7:
Bonner, Michael F; Epstein, Russell A (2018) Computational mechanisms underlying cortical responses to the affordance properties of visual scenes. PLoS Comput Biol 14:e1006111
Julian, Joshua B; Keinath, Alexandra T; Marchette, Steven A et al. (2018) The Neurocognitive Basis of Spatial Reorientation. Curr Biol 28:R1059-R1073
Vass, Lindsay K; Epstein, Russell A (2017) Common Neural Representations for Visually Guided Reorientation and Spatial Imagery. Cereb Cortex 27:1457-1471
Bonner, Michael F; Epstein, Russell A (2017) Coding of navigational affordances in the human visual system. Proc Natl Acad Sci U S A 114:4793-4798
Keinath, Alex T; Julian, Joshua B; Epstein, Russell A et al. (2017) Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation. Curr Biol 27:309-317
Marchette, Steven A; Ryan, Jack; Epstein, Russell A (2017) Schematic representations of local environmental space guide goal-directed navigation. Cognition 158:68-80
Epstein, Russell A; Patai, Eva Zita; Julian, Joshua B et al. (2017) The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 20:1504-1513

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