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In daily life, we often make decisions based on relative value of the options, and we often derive these values from segmenting or integrating the outcomes of past episodes in memory. The neural correlates involved in value-based decision-making have been extensively studied in the literature, but few studies have investigated this topic in decisions that require segmenting or integrating episodic memory from related sources, and even fewer studies examine it in the context of spatial navigation. Building on the computational models from our previous studies, the current study investigates the neural substrates involved in decisions that require people either segment or integrate wayfinding outcomes involving different goals, across virtual spatial navigation tasks with differing demands. We find that when decisions require computation of spatial distances for navigation options, but also evaluation of one's prior spatial navigation ability with the task, the estimated value of navigational choices (EV) modulates neural activity in the dorsomedial prefrontal (dmPFC) cortex and ventrolateral prefrontal (vlFPC) cortex. However, superior parietal cortex tracked EV when decision-making tasks only require spatial distance memory but not evaluation of spatial navigation ability. Our findings reveal divergent neural substrates of memory integration in value-based decision-making under different spatial processing demands., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

The current study investigated how stress affects value-based decision-making during spatial navigation and different types of learning underlying decisions. Eighty-two adult participants (42 females) first learned to find object locations in a virtual environment from a fixed starting location (rigid learning) and then to find the same objects from unpredictable starting locations (flexible learning). Participants then decided whether to reach goal objects from the fixed or unpredictable starting location. We found that stress impairs rigid learning in females, and it does not impair, and even improves, flexible learning when performance with rigid learning is controlled for. Critically, examining how earlier learning influences subsequent decision-making using computational models, we found that stress reduces memory integration, making participants more likely to focus on recent memory and less likely to integrate information from other sources. Collectively, our results show how stress impacts different memory systems and the communication between memory and decision-making.

Reinforcement learning (RL) models have been influential in characterizing human learning and decision making, but few studies apply them to characterizing human spatial navigation and even fewer systematically compare RL models under different navigation requirements. Because RL can characterize one's learning strategies quantitatively and in a continuous manner, and one's consistency of using such strategies, it can provide a novel and important perspective for understanding the marked individual differences in human navigation and disentangle navigation strategies from navigation performance. One-hundred and fourteen participants completed wayfinding tasks in a virtual environment where different phases manipulated navigation requirements. We compared performance of five RL models (3 model-free, 1 model-based and 1 "hybrid") at fitting navigation behaviors in different phases. Supporting implications from prior literature, the hybrid model provided the best fit regardless of navigation requirements, suggesting the majority of participants rely on a blend of model-free (route-following) and model-based (cognitive mapping) learning in such navigation scenarios. Furthermore, consistent with a key prediction, there was a correlation in the hybrid model between the weight on model-based learning (i.e., navigation strategy) and the navigator's exploration vs. exploitation tendency (i.e., consistency of using such navigation strategy), which was modulated by navigation task requirements. Together, we not only show how computational findings from RL align with the spatial navigation literature, but also reveal how the relationship between navigation strategy and a person's consistency using such strategies changes as navigation requirements change., (© 2022. The Author(s).)

Valued-based decision-making has been studied for decades in myriad topics such as consumer spending and gambling, but very rarely in spatial navigation despite the link between the two being highly relevant to survival. Furthermore, how people integrate episodic memories, and what factors are related to the extent of memory integration in value-based decision-making, remain largely unknown. In the current study, participants learned locations of various objects in a virtual environment and then decided whether to reach goal objects from familiar starting locations or unpredictable ones, with different penalties associated with each option. We developed computational models to test whether, when given an object to find, participants' starting location decisions reflected their past performance specific to that goal (Target-specific model) or integrated memory from performance with all goals in the environment (Target-common model). Because participants' wayfinding performance improved throughout the experiment, we were able to examine what factors related to the generalization of past experience. We found that most participants' decisions were better fit by the Target-common model, and for the people whose decisions were better fit by the Target-common model this integrative tendency may be tied to their concurrently greater performance variability with individual targets. Moreover, greater success on our task was predicted by an interaction between the ability to estimate probabilities relevant to decision-making and self-report general task ability. Collectively, our results show how related navigational episodic memories can be reflected in decision-making, and uncover individual differences contributing to such processes. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

When navigating our world we often first plan or retrieve a route to our goal, avoiding alternative paths to other destinations. Inspired by computational and animal models, we have recently demonstrated evidence that the human hippocampus supports prospective spatial coding, mediated by interactions with the prefrontal cortex. But the relationship between such signals and the need to discriminate possible routes based on their goal remains unclear. In the current study, we combined human fMRI, multi-voxel pattern analysis, and an established paradigm for contrasting memories of nonoverlapping routes with those of routes that cross paths and must be disambiguated. By classifying goal-oriented representations at the initiation of a navigational route, we demonstrate that environmental overlap modulates goal-oriented representations in the hippocampus. This modulation manifest through representational shifts from posterior to anterior components of the right hippocampus. Moreover, declines in goal-oriented decoding due to overlapping memories were predicted by the strength of the alternative memory, suggesting co-expression and competition between alternatives in the hippocampus during prospective thought. Moreover, exploratory whole-brain analyses revealed that a region of frontopolar cortex, which we have previously tied to prospective route planning, represented goal-states in new overlapping routes. Together, our findings provide insight into the influences of contextual overlap on the long-axis of the hippocampus and a broader memory and planning network that we have long-associated with such navigation tasks., (© 2022 Wiley Periodicals LLC.)

Objective: This study evaluated whether vestibular dysfunction is associated with reduced spatial navigation performance., Study Design: Cross-sectional study., Setting: Otolaryngology Clinic in the Johns Hopkins Outpatient Center and an analogous virtual reality (VR) environment., Patients: Eligible patients had diagnosis of unilateral or bilateral vestibular loss. Matched healthy controls were recruited at 1:1 ratio., Interventions: The navigation task involved a route-based or place-based strategy in both real world and VR environments., Main Outcome Measures: Navigation performance was measured by distance travelled relative to optimal distance (i.e., path ratio) and the Judgments of Relative Direction (JRD) task, whereby participants had to recall relative angular distances between landmarks., Results: The study sample included 20 patients with vestibular loss (mean age: 61 yrs, SD: 10.2 yrs) and 20 matched controls (mean age: 60 yrs, SD: 10.4 yrs). Patients with vestibular loss travelled significantly greater distance using both route-based (path ratio 1.3 vs. 1.0, p = 0.02) and place-based (path ratio 2.6 vs. 2.0, p = 0.03) strategies in the real world. Overall, participants performed worse in virtual reality compared to real world in both path ratio (2.2 vs. 1.7; p = 0.04) and JRD error (78° vs. 67°; p < 0.01). Furthermore, while controls exhibited significant positive correlations between real world and VR performance in place-based (β = 0.75; p < 0.001) and JRD tasks (β = 0.70; p < 0.001), patients with vestibular loss exhibited no similar correlations., Conclusions: The vestibular system appears to play a role in navigation ability during both actual and virtual navigation, suggesting a role for static vestibular signals in navigation performance., Competing Interests: The authors disclose no conflicts of interest., (Copyright © 2021, Otology & Neurotology, Inc.)

A fundamental question in memory research is how the hippocampus processes contextual cues to retrieve distinct mnemonic associations. Prior research has emphasized the importance of hippocampal-prefrontal interactions for context-dependent memory. Our fMRI study examined the human medial temporal lobes (MTL) and their prefrontal interactions when retrieving memories associated with hierarchically organized task contexts. Participants learned virtual object-location associations governed by subordinate and superordinate task rules, which could be independently cued to change. On each fMRI trial, participants retrieved the correct object for convergent rule and location contextual information. Results demonstrated that hippocampal activity and hippocampal-prefrontal functional interconnectivity distinguished retrieval under different levels of hierarchically organized task rules. In explicit contrast to the hippocampal tail, anterior (body and head) regions were recruited specifically for superordinate changes in the contextual hierarchy. The hippocampal body also differed in its functional connectivity with the prefrontal cortex for superordinate versus subordinate changes. Our findings demonstrate a gradient in MTL for associative retrieval under changing task rules, and advance understanding of hippocampal-prefrontal interactions that support flexible contextual memory., (© 2021 Wiley Periodicals LLC.)

Introduction: We and collaborators discovered that flickering lights and sound at gamma frequency (40 Hz) reduce Alzheimer's disease (AD) pathology and alter immune cells and signaling in mice. To determine the feasibility of this intervention in humans we tested the safety, tolerability, and daily adherence to extended audiovisual gamma flicker stimulation., Methods: Ten patients with mild cognitive impairment due to underlying AD received 1-hour daily gamma flicker using audiovisual stimulation for 4 or 8 weeks at home with a delayed start design., Results: Gamma flicker was safe, tolerable, and adherable. Participants' neural activity entrained to stimulation. Magnetic resonance imaging and cerebral spinal fluid proteomics show preliminary evidence that prolonged flicker affects neural networks and immune factors in the nervous system., Discussion: These findings show that prolonged gamma sensory flicker is safe, tolerable, and feasible with preliminary indications of immune and network effects, supporting further study of gamma stimulation in AD., Competing Interests: Annabelle C. Singer owns shares in Cognito Therapeutics, which aims to develop gamma stimulation‐related products; these conflicts of interest have been disclosed to and are managed by the Georgia Institute of Technology Office of Research Integrity Assurance. Since the completion of this study, Dr. Levey serves as a consultant to Cognito Therapeutics, who provides funding support for this study and manufactures products used in this study. Dr. Levey receives compensation for these services. The terms of this arrangement have been reviewed and approved by Emory University in accordance with its conflict of interest policies. The authors declare no other competing financial interests., (© 2021 The Authors. Alzheimer's & Dementia: Translational Research & Clinical Interventions published by Wiley Periodicals, Inc. on behalf of Alzheimer's Association.)

A substantial amount of research has been conducted to uncover factors underlying the pronounced individual differences in spatial navigation. Spatial working memory capacity (SWM) is shown to be one important factor. In other domains such as reading comprehension, the role of working memory capacity in task performance differences depends on the difficulty of other task demands. In the current study, we investigated whether, similarly, the relationship between SWM and spatial performance was dependent on the difficulty of spatial information integration in the environment. Based on our prior work, spatial information integration difficulty depends on (a) difficulty in observing spatial relationships between locations of interest in the environment and (b) the individual's ability to integrate such relationships. Leveraging virtual reality, we manipulated the difficulty in observing the spatial relationships during learning by changing the visibility of the buildings, and measured individual's self-report sense of direction (SOD) which modulates the ability to integrate such relationships under different degrees of visibility. We consistently found that in the "easy" spatial integration condition (high SOD with high visibility), high SWM did not significantly improve spatial learning. The same pattern was observed in the difficult condition (low SOD with low visibility). On the other hand, high SWM improved spatial learning for medium difficulty (high SOD with low visibility, or vice versa). Together, our results reveal that the role of SWM in spatial learning differences depends on spatial integration difficulty. Our results also have significant applied implications for using virtual reality to target and facilitate spatial learning. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

There has been great interest in how previously acquired knowledge interacts with newly learned knowledge and how prior knowledge facilitates semantic and "schema" learning. In studies of episodic memory, it is broadly associated with interference. Very few studies have examined the balance between interference and facilitation over the course of temporally-extended events and its individual differences. In the present study, we recruited 120 participants for a two-day spatial navigation experiment, wherein participants on Day 2 navigated virtual routes that were learned from Day 1 while also learning new routes. Critically, half of the new mazes overlapped with the old mazes, while the other half did not, enabling us to examine interference and facilitation in the context of spatial episodic learning. Overall, we found that navigation performance in new mazes that overlapped with previously-learned routes was significantly worse than the new non-overlapping mazes, suggesting proactive interference. Interestingly, we found memory facilitation for new routes in familiar environments in locations where there was no direct overlap with the previously-learned routes. Cognitive map accuracy positively correlated with proactive interference. Moreover, participants with high self-report spatial ability and/or a preference for place-based learning experienced more proactive interference. Taken together, our results show that 1) both memory interference and facilitation can co-occur as a function of prior learning, 2) proactive interference within a route varied as a function of the degree of overlap with old knowledge, and 3) individual differences in spatial ability and strategy can modulate proactive interference., (Copyright © 2020 Elsevier B.V. All rights reserved.)

Marked individual differences in the ability to mentally map our environment are pronounced not only among people of different ages or clinical conditions, but also within healthy young adults. Previous studies have shown that hippocampus size positively correlated with spatial navigation ability in healthy young adults, navigation experts, and patients with hippocampus lesions. However, a recent pre-registered study (Weisberg, Newcombe, & Chatterjee, 2019) with a large sample size (n = 90) did not observe this correlation in healthy young adults. Motivated by evidence that self-report sense of direction (SOD) could have a profound impact on how individuals utilize environmental cues, and that different navigation strategies could have opposite impacts on wayfinding performance in individuals with different cognitive map formation (CMF) abilities, we reanalyzed the publicly available dataset from Weisberg et al.'s study. We tested the influence of participants' SOD and CMF abilities on hippocampal volume-performance relationships. We find evidence that the non-significant correlation could envelop heterogeneous correlations among subgroups of individuals: the correlation between the right posterior hippocampal volume and spatial learning performance is significantly higher among individuals with high spatial ability than individuals with low spatial ability. This pattern of performance was observed for both SOD and CMF moderations of the relationship between hippocampal volume and spatial learning. While our re-analyses are fundamentally exploratory in nature, the new results imply that the relationship between hippocampal volume and spatial learning performance might be more complicated than previously thought., (Published by Elsevier Ltd.)

Environmental barriers fundamentally shape our behavior and conceptualization of space [1-5]. Evidence from rodents suggests that, in contrast to an open-field environment, where grid cells exhibit firing patterns with a 6-fold rotational symmetry [5, 6], barriers within the field abolish the 6-fold symmetry and fragment the grid firing fields into compartmentalized repeating "submaps" [5]. These results suggest that barriers may exert their influence on the cognitive map through organization of the metric representation of space provided by entorhinal neurons. We directly tested this hypothesis in humans, combining functional MRI with a virtual navigation paradigm in which we manipulated the local barrier structure. When participants performed a fixed-route foraging task in an open field, the functional MRI signal in right entorhinal cortex exhibited a 6-fold periodic modulation by movement direction associated with conjunctive grid cell firing [7]. However, when environments were compartmentalized by barriers, the grid-like 6-fold spatial metric was abolished. Instead, a 4-fold modulation of the entorhinal signal was observed, consistent with a vectorized organization of spatial metrics predicted by rodent models of navigation [5]. Collectively, these results provide mechanistic insight into why barriers compartmentalize our cognitive map, indicating that boundaries exert a powerful influence on the way environments are represented in human entorhinal cortex. Given that our daily environments are rarely wide open and are often segmented by barriers (e.g., the buildings of our home city), our findings have implications for applying models of cognitive mapping based on grid-like metrics [8] to naturalistic circumstances., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Previous studies from psychology, neuroscience and geography showed that environmental barriers fragment the representation of the environment, reduce spatial navigation efficiency, distort distance estimation and make spatial updating difficult. Despite these negative effects, limited research has examined how to overcome barriers and if individual differences mediate their causes and potential interventions. We hypothesize that the reduced visibility caused by barriers plays a major role in accumulating error in spatial updating and encoding spatial relationships. We tested this using virtual navigation to grant participants 'X-ray' vision during environment encoding (i.e., barriers become translucent) and quantifying cognitive mapping benefits of counteracting fragmented visibility. We found that compared to the participants trained with naturalistic environment visibility, participants trained in the translucent environment had better performance in wayfinding and pointing tasks, which are theorized to measure navigation efficiency and cognitive mapping. Interestingly, these benefits were only observed in participants with high self-report sense of direction. Together, our results provide important insight into (1) how perceptual barrier effects manifest, even when physical fragmentation of space is held constant, (2) establish a novel intervention that can improve spatial learning, and (3) provide evidence that individual differences modulate perceptual barrier effects and the efficacy of such interventions.

In the current study, we investigated the ways in which the acquisition and transfer of spatial knowledge were affected by (a) the type of spatial relations predominately experienced during learning (routes determined by walkways vs. straight-line paths between locations); (b) environmental complexity; and (c) the availability of rotational body-based information. Participants learned the layout of a virtual shopping mall by repeatedly searching for target storefronts located in 1 of the buildings. We created 2 novel learning conditions to encourage participants to use either route knowledge (paths on walkways between buildings) or survey knowledge (straight-line distances and directions from storefront to storefront) to find the target, and measured the development of route and survey knowledge in both learning conditions. Environmental complexity was manipulated by varying the alignment of the buildings with the enclosure, and the visibility within space. Body-based information was manipulated by having participants perform the experiment in front of a computer monitor or using a head-mounted display. After navigation, participants pointed to various storefronts from a fixed position and orientation. Results showed that the frequently used spatial knowledge could be developed similarly across environments with different complexities, but the infrequently used spatial knowledge was less developed in the complex environment. Furthermore, rotational body-based information facilitated spatial learning under certain conditions. Our results suggest that path integration may play an important role in spatial knowledge transfer, both from route to survey knowledge (cognitive map construction), and from survey to route knowledge (using cognitive map to guide wayfinding). (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Previous studies showed that people could use either an egocentric or allocentric reference frame in spatial updating with body-based cues (i.e., physical body movements), but the adopted reference frame was anchored by the physical egocentric front when body-based cues were constrained. A recent study (He et al., 2018) showed that even without body-based cues, the orientation participants initially faced in the virtual environment (VE; initial heading) could be used to establish a reference frame, suggesting that the physical egocentric front could be overridden by a virtual orientation. In the current project, we aimed to: (a) replicate He et al.'s (2018) finding; (b) examine when the reference frame defined by the virtual initial heading was established; and (c) investigate the cognitive processes in establishing the initial heading as a reference frame. In four experiments, we were able to replicate the previous findings and found that the reference frame defined by the initial heading was established during spatial updating. More importantly, the reference frame defined by the initial heading was egocentric and participants did not need to know the orientation of their initial heading at the beginning of spatial updating to be able to use it. We discuss the cognitive processes of reference frame selection in spatial updating when body-based cues are absent.

This study investigated how spatial updating strategies affected the selection of reference frames in path integration. Participants walked an outbound path consisting of three successive waypoints in a featureless environment and then pointed to the first waypoint. We manipulated the alignment of participants' final heading at the end of the outbound path with their initial heading to examine the adopted reference frame. We assumed that the initial heading defined the principal reference direction in an allocentric reference frame. In Experiment 1, participants were instructed to use a configural updating strategy and to monitor the shape of the outbound path while they walked it. Pointing performance was best when the final heading was aligned with the initial heading, indicating the use of an allocentric reference frame. In Experiment 2, participants were instructed to use a continuous updating strategy and to keep track of the location of the first waypoint while walking the outbound path. Pointing performance was equivalent regardless of the alignment between the final and the initial headings, indicating the use of an egocentric reference frame. These results confirmed that people could employ different spatial updating strategies in path integration (Wiener, Berthoz, & Wolbers Experimental Brain Research 208(1) 61-71, 2011), and suggested that these strategies could affect the selection of the reference frame for path integration.

The current study investigated the reference frame used in spatial updating when idiothetic cues to self-motion were minimized (desktop virtual reality). In Experiment 1, participants learned a layout of eight objects from a single perspective (learning heading) in a virtual environment. After learning, they were placed in the same virtual environment and used a keyboard to navigate to two of the learned objects (visible) before pointing to a third object (invisible). We manipulated participants' starting orientation (initial heading) and final orientation (final heading) before pointing, to examine the reference frame used in this task. We found that participants used the initial heading and the learning heading to establish reference directions. In Experiment 2, the procedure was almost the same as in Experiment 1 except that participants pointed to objects relative to an imagined heading that differed from their final heading in the virtual environment. In this case, pointing performance was only affected by alignment with the learning heading. We concluded that the initial heading played an important role in spatial updating without idiothetic cues, but the representation established at this heading was transient and affected by the interruption of spatial updating; the learning heading, on the other hand, corresponded to an enduring representation which was used consistently.

Accurate wayfinding is essential to the survival of many animal species and requires the ability to maintain spatial orientation during locomotion. One of the ways that humans and other animals stay spatially oriented is through path integration, which operates by integrating self-motion cues over time, providing information about total displacement from a starting point. The neural substrate of path integration in mammals may exist in grid cells, which are found in dorsomedial entorhinal cortex and presubiculum and parasubiculum in rats. Grid cells have also been found in mice, bats, and monkeys, and signatures of grid cell activity have been observed in humans. We demonstrate that distance estimation by humans during path integration is sensitive to geometric deformations of a familiar environment and show that patterns of path integration error are predicted qualitatively by a model in which locations in the environment are represented in the brain as phases of arrays of grid cells with unique periods and decoded by the inverse mapping from phases to locations. The periods of these grid networks are assumed to expand and contract in response to expansions and contractions of a familiar environment. Biases in distance estimation occur when the periods of the encoding and decoding grids differ. Our findings explicate the way in which grid cells could function in human path integration., (Copyright © 2015 Elsevier Ltd. All rights reserved.)