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In familiar environments, the firing fields of entorhinal grid cells form regular triangular lattices. However, when the geometric shape of the environment is deformed, these time-averaged grid patterns are distorted in a grid scale-dependent and local manner. We hypothesized that this distortion in part reflects dynamic anchoring of the grid code to displaced boundaries, possibly through border cell-grid cell interactions. To test this hypothesis, we first reanalyzed two existing rodent grid rescaling datasets to identify previously unrecognized boundary-tethered shifts in grid phase that contribute to the appearance of rescaling. We then demonstrated in a computational model that boundary-tethered phase shifts, as well as scale-dependent and local distortions of the time-averaged grid pattern, could emerge from border-grid interactions without altering inherent grid scale. Together, these results demonstrate that environmental deformations induce history-dependent shifts in grid phase, and implicate border-grid interactions as a potential mechanism underlying these dynamics.more » « less
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Abstract Place and grid cells in the hippocampal formation are commonly thought to support a unified and coherent cognitive map of space. This mapping mechanism faces a challenge when a navigator is placed in a familiar environment that has been deformed from its original shape. Under such circumstances, many transformations could plausibly serve to map a navigator's familiar cognitive map to the deformed space. Previous empirical results indicate that the firing fields of rodent place and grid cells stretch or compress in a manner that approximately matches the environmental deformation, and human spatial memory exhibits similar distortions. These effects have been interpreted as evidence that reshaping a familiar environment elicits an analogously reshaped cognitive map. However, recent work has suggested an alternative explanation, whereby deformation‐induced distortions of the grid code are attributable to a mechanism that dynamically anchors grid fields to the most recently experienced boundary, thus causing history‐dependent shifts in grid phase. This interpretation raises the possibility that human spatial memory will exhibit similar history‐dependent dynamics. To test this prediction, we taught participants the locations of objects in a virtual environment and then probed their memory for these locations in deformed versions of this environment. Across three experiments with variable access to visual and vestibular cues, we observed the predicted pattern, whereby the remembered locations of objects were shifted from trial to trial depending on the boundary of origin of the participant's movement trajectory. These results provide evidence for a dynamic anchoring mechanism that governs both neuronal firing and spatial memory.
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Abstract Rodent lesion studies have revealed the existence of two causally dissociable spatial memory systems, localized to the hippocampus and striatum that are preferentially sensitive to environmental boundaries and landmark objects, respectively. Here we test whether these two memory systems are causally dissociable in humans by examining boundary‐ and landmark‐based memory in typical and atypical development. Adults with Williams syndrome (
WS )—a developmental disorder with known hippocampal abnormalities—and typical children and adults, performed a navigation task that involved learning locations relative to a boundary or a landmark object. We found that boundary‐based memory was severely impaired inWS compared to typically‐developing mental‐age matched (MA ) children and chronological‐age matched (CA ) adults, whereas landmark‐based memory was similar in all groups. Furthermore, landmark‐based memory matured earlier in typical development than boundary‐based memory, consistent with the idea that theWS cognitive phenotype arises from developmental arrest of late maturing cognitive systems. Together, these findings provide causal and developmental evidence for dissociable spatial memory systems in humans.