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Spatial navigation deficits are often observed among older adults on tasks that require navigating virtual reality (VR) environments on a computer screen. We investigated whether these age differences are attenuated when tested in more naturalistic and ambulatory virtual environments. In Experiment 1, young and older adults navigated a variant of the Morris Water Maze task in each of two VR conditions: a desktop VR condition which required using a mouse and keyboard to navigate, and an ambulatory VR condition which permitted unrestricted locomotion. In Experiment 2, we examined whether age- and VR-related differences in spatial performance were affected by the inclusion of additional spatial cues. In both experiments, older adults navigated to target locations less precisely than younger individuals in the desktop condition. Age differences were significantly attenuated, however, when tested in the ambulatory VR environment. These findings underscore the importance of developing naturalistic assessments of spatial memory and navigation.

Previous work has shown how different interfaces (i.e., route navigation, maps, or a combination of the two) influence spatial knowledge and recollection. To test for the existence of intermediate representations along an egocentric-to-allocentric continuum, we developed a novel task, tabletop navigation, to provide a mixture of cues that inform the emergence of egocentric and allocentric representations or strategies. In this novel tabletop task, participants navigated a remote-controlled avatar through a tabletop scale model of the virtual city. Participants learned virtual cities from either navigating routes, studying maps, or our new tabletop navigation task. We interleaved these learning tasks with either an in situ pointing task (the scene- and orientation-dependent pointing [SOP] task) or imagined judgements of relative direction (JRD) pointing. In Experiment 1, performance on each memory task was similar across learning tasks and performance on the route and map learning tasks correlated with more precise spatial recall on both the JRD and SOP tasks. Tabletop learning performance correlated with SOP performance only, suggesting a reliance on egocentric strategies, although increased utilization of the affordances of the tabletop task were related to JRD performance. In Experiment 2, using a modified criterion map learning task, participants who learned using maps provided more precise responses on the JRD compared to route or tabletop learning. Together, these findings provide mixed evidence for both optimization and egocentric predominance after learning from the novel tabletop navigation task., (© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Spatial navigation and memory are often seen as heavily intertwined at the cognitive and neural levels of analysis. We review models that hypothesize a central role for the medial temporal lobes, including the hippocampus, in both navigation and aspects of memory, particularly allocentric navigation and episodic memory. While these models have explanatory power in instances in which they overlap, they are limited in explaining functional and neuroanatomical differences. Focusing on human cognition, we explore the idea of navigation as a dynamically acquired skill and memory as an internally driven process, which may better account for the differences between the two. We also review network models of navigation and memory, which place a greater emphasis on connections rather than the functions of focal brain regions. These models, in turn, may have greater explanatory power for the differences between navigation and memory and the differing effects of brain lesions and age., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

An important question regards the nature of our spatial memories for the paths that we have walked and, in particular, whether such distortions might violate the topological properties of the shape of the paths (i.e., creating an intersection when two paths did not intersect or vice versa). To investigate whether and how this might occur, we tested humans in situations in which they walked simple paths and idiothetic and visual cues either matched or mismatched, with the mismatching cues creating the greatest potential for topological distortions. Participants walked four-segment paths with 90° turns in immersive virtual reality and pointed to their start location when they arrived at the end of the path. In paths with a crossing, when the intersection was not presented, participants pointed to a novel start location suggesting a topological distortion involving non-crossed paths. In paths without a crossing, when a false intersection was presented, participants pointed to a novel start location suggesting a topological distortion involving crossed paths. In paths without crossings and without false intersections, participants showed reduced pointing errors that typically did not involve topological distortions. Distortions more generally, as indicated by pointing errors to the start location, were significantly reduced for walked paths involving primarily idiothetic cues with limited visual cues; conversely, distortions were significantly increased when idiothetic cues were diminished and navigation relied primarily on visual cues. Our findings suggest that our spatial memories for walked paths sometimes involve topological distortions, particularly when resolving the competition between idiothetic and visual cues., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Du et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Spatial navigation and event memory (termed episodic memory) are thought to be heavily intertwined, both in terms of their cognitive processes and underlying neural systems. Some theoretical models posit that both memory for places during navigation and episodic memory depend on highly overlapping brain systems. Here, we assessed this relationship by testing navigation in an individual with severe retrograde and anterograde amnesia; the amnesia stemmed from bilateral lesions in the medial temporal lobes from two separate strokes. The individual with amnesia and age-matched controls were tested on their memories for the locations of previously seen objects relative to distal mountain cues in an immersive virtual environment involving free ambulation. All participants were tested from both repeated and novel start locations and when a single distal mountain cue was unknowingly moved to determine if they relied on a single (beacon) cue to a greater extent than the collection of all distal cues. Compared to age-matched controls, the individual with amnesia showed no significant deficits in navigation from either the repeated or novel start points, although both the individual with amnesia and controls performed well above chance at placing objects near their correct locations. The individual with amnesia also relied on a combination of distal cues in a manner comparable to age-matched controls. Despite largely intact memory for locations using distal cues, the individual with amnesia walked longer paths, rotated more, and took longer to complete trials. Our findings suggest that memory for places during navigation and episodic memory may involve partially dissociable brain circuits and that other brain regions outside of the medial temporal lobe partially support some aspects of navigation. At the same time, the fact that the individual with amnesia walked more circuitous paths and had dense amnesia for autobiographic events supports the idea that the hippocampus may be important for binding information as part of a larger role in memory., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

A critical question regards the neural basis of complex cognitive skill acquisition. One extensively studied skill is navigation, with evidence suggesting that humans vary widely in navigation abilities. Yet, data supporting the neural underpinning of these individual differences are mixed. Some evidence suggests robust structure-behavior relations between hippocampal volume and navigation ability, whereas other experiments show no such correlation. We focus on several possibilities for these discrepancies: 1) volumetric hippocampal changes are relevant only at the extreme ranges of navigational abilities; 2) hippocampal volume correlates across individuals but only for specific measures of navigation skill; 3) hippocampal volume itself does not correlate with navigation skill acquisition; connectivity patterns are more relevant. To explore this third possibility, we present a model emphasizing functional connectivity changes, particularly to extra-hippocampal structures. This class of models arises from the premise that navigation is dynamic and that good navigators flexibly solve spatial challenges. These models pave the way for research on other skills and provide more precise predictions for the neural basis of skill acquisition., (Copyright © 2021 Elsevier Ltd. All rights reserved.)

Research into the behavioral and neural correlates of spatial cognition and navigation has benefited greatly from recent advances in virtual reality (VR) technology. Devices such as head-mounted displays (HMDs) and omnidirectional treadmills provide research participants with access to a more complete range of body-based cues, which facilitate the naturalistic study of learning and memory in three-dimensional (3D) spaces. One limitation to using these technologies for research applications is that they almost ubiquitously require integration with video game development platforms, also known as game engines. While powerful, game engines do not provide an intrinsic framework for experimental design and require at least a working proficiency with the software and any associated programming languages or integrated development environments (IDEs). Here, we present a new asset package, called Landmarks, for designing and building 3D navigation experiments in the Unity game engine. Landmarks combines the ease of building drag-and-drop experiments using no code, with the flexibility of allowing users to modify existing aspects, create new content, and even contribute their work to the open-source repository via GitHub, if they so choose. Landmarks is actively maintained and is supplemented by a wiki with resources for users including links, tutorials, videos, and more. We compare several alternatives to Landmarks for building navigation experiments and 3D experiments more generally, provide an overview of the package and its structure in the context of the Unity game engine, and discuss benefits relating to the ongoing and future development of Landmarks.

Moving our body through space is fundamental to human navigation; however, technical and physical limitations have hindered our ability to study the role of these body-based cues experimentally. We recently designed an experiment using novel immersive virtual-reality technology, which allowed us to tightly control the availability of body-based cues to determine how these cues influence human spatial memory [Huffman, D. J., & Ekstrom, A. D. A modality-independent network underlies the retrieval of large-scale spatial environments in the human brain. Neuron , 104 , 611-622, 2019]. Our analysis of behavior and fMRI data revealed a similar pattern of results across a range of body-based cues conditions, thus suggesting that participants likely relied primarily on vision to form and retrieve abstract, holistic representations of the large-scale environments in our experiment. We ended our paper by discussing a number of caveats and future directions for research on the role of body-based cues in human spatial memory. Here, we reiterate and expand on this discussion, and we use a commentary in this issue by A. Steel, C. E. Robertson, and J. S. Taube (Current promises and limitations of combined virtual reality and functional magnetic resonance imaging research in humans: A commentary on Huffman and Ekstrom (2019). Journal of Cognitive Neuroscience , 2020) as a helpful discussion point regarding some of the questions that we think will be the most interesting in the coming years. We highlight the exciting possibility of taking a more naturalistic approach to study the behavior, cognition, and neuroscience of navigation. Moreover, we share the hope that researchers who study navigation in humans and nonhuman animals will synergize to provide more rapid advancements in our understanding of cognition and the brain.

A recent study in humans shows that stress increases our reliance on familiar routes during navigation. This research explains how increases in cortisol, a biomarker of stress, disrupts navigation-related brain circuits, resulting in less efficient navigation., (Copyright © 2020 Elsevier Inc. All rights reserved.)

Path integration is thought to rely on vestibular and proprioceptive cues yet most studies in humans involve primarily visual input, providing limited insight into their respective contributions. We developed a paradigm involving walking in an omnidirectional treadmill in which participants were guided on two sides of a triangle and then found their back way to origin. In Experiment 1, we tested a range of different triangle types while keeping the distance of the unguided side constant to determine the influence of spatial geometry. Participants overshot the angle they needed to turn and undershot the distance they needed to walk, with no consistent effect of triangle type. In Experiment 2, we manipulated distance while keeping angle constant to determine how path integration operated over both shorter and longer distances. Participants underestimated the distance they needed to walk to the origin, with error increasing as a function of the walked distance. To attempt to account for our findings, we developed configural-based computational models involving vector addition, the second of which included terms for the influence of past trials on the current one. We compared against a previously developed configural model of human path integration, the Encoding-Error model. We found that the vector addition models captured the tendency of participants to under-encode guided sides of the triangles and an influence of past trials on current trials. Together, our findings expand our understanding of body-based contributions to human path integration, further suggesting the value of vector addition models in understanding these important components of human navigation., Competing Interests: The authors have declared that no competing interests exist.

Grid cells provide a compelling example of a link between cellular activity and an abstract and difficult to define concept like space. Accordingly, a representational perspective on grid coding argues that neural grid coding underlies a fundamentally spatial metric. Recently, some theoretical proposals have suggested extending such a framework to nonspatial cognition as well, such as category learning. Here, we provide a critique of the frequently employed assumption of an isomorphism between patterns of neural activity (e.g., grid cells), mental representation, and behavior (e.g., navigation). Specifically, we question the strict isomorphism between these three levels and suggest that human spatial navigation is perhaps best characterized by a wide variety of both metric and nonmetric strategies. We offer an alternative perspective on how grid coding might relate to human spatial navigation, arguing that grid coding is part of a much larger conglomeration of neural activity patterns that dynamically tune to accomplish specific behavioral outputs., (© 2019 Wiley Periodicals, Inc.)

In humans, the extent to which body-based cues, such as vestibular, somatosensory, and motoric cues, are necessary for normal expression of spatial representations remains unclear. Recent breakthroughs in immersive virtual reality technology allowed us to test how body-based cues influence spatial representations of large-scale environments in humans. Specifically, we manipulated the availability of body-based cues during navigation using an omnidirectional treadmill and a head-mounted display, investigating brain differences in levels of activation (i.e., univariate analysis), patterns of activity (i.e., multivariate pattern analysis), and putative network interactions between spatial retrieval tasks using fMRI. Our behavioral and neuroimaging results support the idea that there is a core, modality-independent network supporting spatial memory retrieval in the human brain. Thus, for well-learned spatial environments, at least in humans, primarily visual input may be sufficient for expression of complex representations of spatial environments. VIDEO ABSTRACT., (Copyright © 2019 Elsevier Inc. All rights reserved.)

An important question regards how we use environmental boundaries to anchor spatial representations during navigation. Behavioral and neurophysiological models appear to provide conflicting predictions, and this question has been difficult to answer because of technical challenges with testing navigation in novel, large-scale, realistic spatial environments. We conducted an experiment in which participants freely ambulated on an omnidirectional treadmill while viewing novel, town-sized environments in virtual reality on a head-mounted display. Participants performed interspersed judgments of relative direction (JRD) to assay their spatial knowledge and to determine when during learning they employed environmental boundaries to anchor their spatial representations. We designed JRD questions that assayed directions aligned and misaligned with the axes of the surrounding rectangular boundaries and employed structural equation modeling to better understand the learning-dependent dynamics for aligned versus misaligned pointing. Pointing accuracy showed no initial directional bias to boundaries, although such "alignment effects" did emerge after the fourth block of learning. Preexposure to a map in Experiment 2 led to similar overall findings. A control experiment in which participants studied a map but did not navigate the environment, however, demonstrated alignment effects after a brief, initial learning experience. Our results help to bridge the gap between neurophysiological models of location-specific firing in rodents and human behavioral models of spatial navigation by emphasizing the experience-dependent accumulation of route-specific knowledge. In particular, our results suggest that the use of spatial boundaries as an organizing schema during navigation of large-scale space occurs in an experience-dependent fashion. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Numerous reports have demonstrated low-frequency oscillations during navigation using invasive recordings in the hippocampus of both rats and human patients. Given evidence, in some cases, of low-frequency synchronization between midline cortex and hippocampus, it is also possible that low-frequency movement-related oscillations manifest in healthy human neocortex. However, this possibility remains largely unexplored, in part due to the difficulties of coupling free ambulation and effective scalp EEG recordings. In the current study, participants freely ambulated on an omnidirectional treadmill and explored an immersive virtual reality city rendered on a head-mounted display while undergoing simultaneous wireless scalp EEG recordings. We found that frontal-midline (FM) delta-theta (2-7.21 Hz) oscillations increased during movement compared to standing still periods, consistent with a role in navigation. In contrast, posterior alpha (8.32-12.76 Hz) oscillations were suppressed in the presence of visual input, independent of movement. Our findings suggest that FM delta-theta and posterior alpha oscillations arise at independent frequencies, under complementary behavioral conditions, and, at least for FM delta-theta oscillations, at independent recordings sites. Together, our findings support a double dissociation between movement-related FM delta-theta and resting-related posterior alpha oscillations. Our study thus provides novel evidence that FM delta-theta oscillations arise, in part, from real-world ambulation, and are functionally independent from posterior alpha oscillations., (© 2018 Society for Psychophysiological Research.)

Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding., Significance Statement: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation., (© 2017 Wiley Periodicals, Inc.)

Navigation is an inherently dynamic and multimodal process, making isolation of the unique cognitive components underlying it challenging. The assumptions of much of the literature on human spatial navigation are that 1) spatial navigation involves modality independent, discrete metric representations (i.e., egocentric vs. allocentric), 2) such representations can be further distilled to elemental cognitive processes, and 3) these cognitive processes can be ascribed to unique brain regions. We argue that modality-independent spatial representations, instead of providing exact metrics about our surrounding environment, more often involve heuristics for estimating spatial topology useful to the current task at hand. We also argue that egocentric (body centered) and allocentric (world centered) representations are better conceptualized as involving a continuum rather than as discrete. We propose a neural model to accommodate these ideas, arguing that such representations also involve a continuum of network interactions centered on retrosplenial and posterior parietal cortex, respectively. Our model thus helps explain both behavioral and neural findings otherwise difficult to account for with classic models of spatial navigation and memory, providing a testable framework for novel experiments.

Low-Frequency Oscillations (LFO) in the range of 7-9 Hz, or theta rhythm, has been recorded in rodents ambulating in the real world. However, intra-hippocampus EEG recordings during virtual navigation in humans have consistently reported LFO that appear to predominate around 3-4 Hz. Here we report clear evidence of 7-9 Hz rhythmicity in raw intra-hippocampus EEG traces during real as well as virtual movement. Oscillations typically occur at a lower frequency in virtual than real world navigation. This study highlights the possibility that human and rodent hippocampal EEG activity are not as different as previously reported and this difference may arise, in part, due to the lack of actual movement in previous human navigation studies, which were virtual.

Mental simulation is a hallmark feature of human cognition, allowing features from memories to be flexibly used during prospection. While past studies demonstrate the preservation of real-world features such as size and distance during mental simulation, their temporal dynamics remains unknown. Here, we compare mental simulations to navigation of routes in a large-scale spatial environment to test the hypothesis that such simulations are temporally compressed in an adaptive manner. Our results show that simulations occurred at 2.39× the speed it took to navigate a route, increasing in compression (3.57×) for slower movement speeds. Participant self-reports of vividness and spatial coherence of simulations also correlated strongly with simulation duration, providing an important link between subjective experiences of simulated events and how spatial representations are combined during prospection. These findings suggest that simulation of spatial events involve adaptive temporal mechanisms, mediated partly by the fidelity of memories used to generate the simulation., (Copyright © 2016 Elsevier B.V. All rights reserved.)

Low-frequency (delta/theta band) hippocampal neural oscillations play prominent roles in computational models of spatial navigation, but their exact function remains unknown. Some theories propose they are primarily generated in response to sensorimotor processing, while others suggest a role in memory-related processing. We directly recorded hippocampal EEG activity in patients undergoing seizure monitoring while they explored a virtual environment containing teleporters. Critically, this manipulation allowed patients to experience movement through space in the absence of visual and self-motion cues. The prevalence and duration of low-frequency hippocampal oscillations were unchanged by this manipulation, indicating that sensorimotor processing was not required to elicit them during navigation. Furthermore, the frequency-wise pattern of oscillation prevalence during teleportation contained spatial information capable of classifying the distance teleported. These results demonstrate that movement-related sensory information is not required to drive spatially informative low-frequency hippocampal oscillations during navigation and suggest a specific function in memory-related spatial updating., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Damage to the medial temporal lobes produces profound amnesia, greatly impairing the ability of patients to learn about new associations and events. While studies in rodents suggest a strong link between damage to the hippocampus and the ability to navigate using distal landmarks in a spatial environment, the connection between navigation and memory in humans remains less clear. Past studies on human navigation have provided mixed findings about whether patients with damage to the medial temporal lobes can successfully acquire and navigate new spatial environments, possibly due, in part, to issues related to patient demographics and characterization of medial temporal lobe damage. Here, we report findings from a young, high functioning patient who suffered severe medial temporal lobe damage. Although the patient is densely amnestic, her ability to acquire and utilize new, but coarse, spatial "maps" appears largely intact. Specifically, a novel computational analysis focused on the precision of her spatial search revealed a significant deficit in spatial precision rather than spatial search strategy. These findings argue that an intact hippocampus in humans is not necessary for representing multiple external landmarks during spatial navigation of new environments. We suggest instead that the human hippocampus may store and represent complex high-resolution bindings of features in the environment as part of a larger role in perception, memory, and navigation., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Place cells are a fundamental component of the rodent navigational system. One intriguing implication of place cells is that humans, by extension, have "map-like" (or GPS-like) knowledge that we use to represent space. Here, we review both behavioral and neural studies of human navigation, suggesting that how we process visual information forms a critical component of how we represent space. These include cellular and brain systems devoted to coding visual information during navigation in addition to a location coding system similar to that described in rodents. Together, these findings suggest that while it is highly useful to think of our navigation system involving internal "maps," we should not neglect the importance of high-resolution visual representations to how we navigate space., (© 2015 Wiley Periodicals, Inc.)

An important, but as yet incompletely resolved, issue is whether spatial knowledge acquired during navigation differs significantly from that acquired by studying a cartographic map. This, in turn, is relevant to understanding the generalizability of the concept of a "cognitive map," which is often likened to a cartographic map. On the basis of previous theoretical proposals, we hypothesized that route and cartographic map learning would produce differences in the dynamics of acquisition of landmark-referenced (allocentric) knowledge, relative to view-referenced (egocentric) knowledge. We compared this model with competing predictions from two other models linked to route versus map learning. To test these ideas, participants repeatedly performed a judgment of relative direction (JRD) and a scene- and orientation-dependent pointing (SOP) task while undergoing route and cartographic map learning of virtual spatial environments. In Experiment 1, we found that map learning led to significantly faster improvements in JRD pointing accuracy than did route learning. In Experiment 2, in contrast, we found that route learning led to more immediate and greater improvements overall in SOP accuracy, as compared to map learning. Comparing Experiments 1 and 2, we found a significant three-way interaction effect, indicating that improvements in performance differed for the JRD versus the SOP task as a function of route versus map learning. We interpreted these findings as suggesting that the learning modality differentially affects the dynamics of how we utilize primarily landmark-referenced versus view-referenced knowledge, suggesting potential differences in how we utilize spatial representations acquired from routes versus cartographic maps.

Experiments on rodents have demonstrated that transecting the white matter fibre pathway linking the hippocampus with an array of cortical and subcortical structures - the fornix - impairs flexible navigational learning in the Morris Water Maze (MWM), as well as similar spatial learning tasks. While diffusion magnetic resonance imaging (dMRI) studies in humans have linked inter-individual differences in fornix microstructure to episodic memory abilities, its role in human spatial learning is currently unknown. We used high-angular resolution diffusion MRI combined with constrained spherical deconvolution-based tractography, to ask whether inter-individual differences in fornix microstructure in healthy young adults would be associated with spatial learning in a virtual reality navigation task. To efficiently capture individual learning across trials, we adopted a novel curve fitting approach to estimate a single index of learning rate. We found a statistically significant correlation between learning rate and the microstructure (mean diffusivity) of the fornix, but not that of a comparison tract linking occipital and anterior temporal cortices (the inferior longitudinal fasciculus, ILF). Further, this correlation remained significant when controlling for both hippocampal volume and participant gender. These findings extend previous animal studies by demonstrating the functional relevance of the fornix for human spatial learning in a virtual reality environment, and highlight the importance of a distributed neuroanatomical network, underpinned by key white matter pathways, such as the fornix, in complex spatial behaviour.

Humans, like many other species, employ three fundamental forms of strategies to navigate: allocentric, egocentric, and beacon. Here, we review each of these different forms of navigation with a particular focus on how our high-resolution visual system contributes to their unique properties. We also consider how we might employ allocentric and egocentric representations, in particular, across different spatial dimensions, such as 1-D vs. 2-D. Our high acuity visual system also leads to important considerations regarding the scale of space we are navigating (e.g., smaller, room-sized "vista" spaces or larger city-sized "environmental" spaces). We conclude that a hallmark of human spatial navigation is our ability to employ these representations systems in a parallel and flexible manner, which differ both as a function of dimension and spatial scale.

Damage to the medial temporal lobes produces profound amnesia, greatly impairing the ability of patients to learn about new associations and events. While studies in rodents suggest a strong link between damage to the hippocampus and the ability to navigate using distal landmarks in a spatial environment, the connection between navigation and memory in humans remains less clear. Past studies on human navigation have provided mixed findings about whether patients with damage to the medial temporal lobes can successfully acquire and navigate new spatial environments, possibly due, in part, to issues related to patient demographics and characterization of medial temporal lobe damage. Here, we report findings from a young, high functioning patient who suffered severe medial temporal lobe damage. Although the patient is densely amnestic, her ability to acquire and utilize new, but coarse, spatial "maps" appears largely intact. Specifically, a novel computational analysis focused on the precision of her spatial search revealed a significant deficit in spatial precision rather than spatial search strategy. These findings argue that an intact hippocampus in humans is not necessary for representing multiple external landmarks during spatial navigation of new environments. We suggest instead that the human hippocampus may store and represent complex high-resolution bindings of features in the environment as part of a larger role in perception, memory, and navigation.

While the widely studied allocentric spatial representation holds a special status in neuroscience research, its exact nature and neural underpinnings continue to be the topic of debate, particularly in humans. Here, based on a review of human behavioral research, we argue that allocentric representations do not provide the kind of map-like, metric representation one might expect based on past theoretical work. Instead, we suggest that almost all tasks used in past studies involve a combination of egocentric and allocentric representation, complicating both the investigation of the cognitive basis of an allocentric representation and the task of identifying a brain region specifically dedicated to it. Indeed, as we discuss in detail, past studies suggest numerous brain regions important to allocentric spatial memory in addition to the hippocampus, including parahippocampal, retrosplenial, and prefrontal cortices. We thus argue that although allocentric computations will often require the hippocampus, particularly those involving extracting details across temporally specific routes, the hippocampus is not necessary for all allocentric computations. We instead suggest that a non-aggregate network process involving multiple interacting brain areas, including hippocampus and extra-hippocampal areas such as parahippocampal, retrosplenial, prefrontal, and parietal cortices, better characterizes the neural basis of spatial representation during navigation. According to this model, an allocentric representation does not emerge from the computations of a single brain region (i.e., hippocampus) nor is it readily decomposable into additive computations performed by separate brain regions. Instead, an allocentric representation emerges from computations partially shared across numerous interacting brain regions. We discuss our non-aggregate network model in light of existing data and provide several key predictions for future experiments.

Humans possess a unique ability to communicate spatially-relevant information, yet the intersection between language and navigation remains largely unexplored. One possibility is that verbal cues accentuate heuristics useful for coding spatial layouts, yet this idea remains largely untested. We test the idea that verbal cues flexibly accentuate the coding of heuristics to remember spatial layouts via spatial boundaries or landmarks. The alternative hypothesis instead conceives of encoding during navigation as a step-wise process involving binding lower-level features, and thus subsequently formed spatial representations should not be modified by verbal cues. Across three experiments, we found that verbal cues significantly affected pointing error patterns at axes that were aligned with the verbally cued heuristic, suggesting that verbal cues influenced the heuristics employed to remember object positions. Further analyses suggested evidence for a hybrid model, in which boundaries were encoded more obligatorily than landmarks, but both were accessed flexibly with verbal instruction. These findings could not be accounted for by a tendency to spend more time facing the instructed component during navigation, ruling out an attentional-encoding mechanism. Our findings argue that verbal cues influence the heuristics employed to code environments, suggesting a mechanism for how humans use language to communicate navigationally-relevant information. [ABSTRACT FROM AUTHOR]

In recent years, the field has reached an impasse between models suggesting that the hippocampus is fundamentally involved in spatial processing and models suggesting that the hippocampus automatically encodes all dimensions of experience in the service of memory. Here, we consider key conceptual issues that have impeded progress in our understanding of hippocampal function, and we review findings that establish the scope and limits of hippocampal involvement in navigation and memory. We argue that space and time serve as a primary scaffold to break up experiences into specific contexts, and to organize multimodal input that is to be associated within a context. However, the hippocampus is clearly capable of incorporating additional dimensions into the scaffold if they are determined to be relevant in the event‐defined context. Conceiving of the hippocampal representation as constrained by immediate task demands—yet preferring axes that involve space and time—helps to reconcile an otherwise disparate set of findings on the core function of the hippocampus. [ABSTRACT FROM AUTHOR]

Abstract: A prominent and replicated finding is the correlation between running speed and increases in low-frequency oscillatory activity in the hippocampal local field potential. A more recent finding concerns low-frequency oscillations that increase in coherence between the hippocampus and neocortical brain areas such as prefrontal cortex during memory-related behaviors (i.e., remembering the correct location to visit). In this review, we tie together movement-related and memory-related low-frequency oscillations in the rodent with similar findings in humans. We argue that although movement-related low-frequency oscillations, in particular, may have slightly different characteristics in humans than rodents, placing important constraints on our thinking about this issue, both phenomena have similar functional foundations. We review four prominent theoretical models that provide partially conflicting accounts of movement-related low-frequency oscillations. We attempt to tie together these theoretical proposals, and existing data in rodents and humans, with memory-related low-frequency oscillations. We propose that movement-related low-frequency oscillations and memory-related low-frequency oscillatory activity, both of which show significant coherence with oscillations in other brain regions, represent different facets of “spectral fingerprints,” or different resonant frequencies within the same brain networks underlying different cognitive processes. Together, movement-related and memory-related low-frequency oscillatory coupling may be linked by their distinct contributions to bottom-up, sensorimotor driven processing and top-down, controlled processing characterizing aspects of memory encoding and retrieval. [Copyright &y& Elsevier]

ABSTRACT Rhythmic oscillations within the 3-12 Hz theta frequency band manifest in the rodent hippocampus during a variety of behaviors and are particularly well characterized during spatial navigation. In contrast, previous studies of rhythmic hippocampal activity in primates under comparable behavioral conditions suggest it may be less apparent and possibly less prevalent, or even absent, compared with the rodent. We compared the relative presence of low-frequency oscillations in rats and humans during spatial navigation by using an oscillation detection algorithm ('P-episode' or 'BOSC') to better characterize their presence in microelectrode local field potential (LFP) recordings. This method quantifies the proportion of time the LFP exceeds both a power and cycle duration threshold at each frequency, characterizing the presence of (1) oscillatory activity compared with background noise, (2) the peak frequency of oscillatory activity, and (3) the duration of oscillatory activity. Results demonstrate that both humans and rodents have hippocampal rhythmic fluctuations lasting, on average, 2.75 and 4.3 cycles, respectively. Analyses further suggest that human hippocampal rhythmicity is centered around ∼3 Hz while that of rats is centered around ∼8 Hz. These results establish that low-frequency rhythms relevant to spatial navigation are present in both the rodent and human hippocampus, albeit with different properties under the behavioral conditions tested. © 2013 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]