认知地图作为人对人地关系复杂系统进行抽象化和秩序化的内在表征,是个体空间行为决策、空间认知与空间规划的理论基础,也是地理学的重要研究领域之一。论文通过CiteSpace文献学分析方法并结合经典文献回顾,从多学科视角系统梳理认知地图1948—2020年共70余年的发展脉络与研究热点。研究认为,认知地图在地理学的学科发展过程中扮演了重要角色,特别是在认知空间与城市意象、空间扭曲与空间偏好、空间知识与决策行为等方面丰富了地理学内涵。近期与地理学有关的认知地图跨学科研究出现3大转向：大数据时代重新定义认知空间与城市意象的数字转向,以特定群体或事件的空间偏好为切入点的情感转向,以第一人称视角解译空间知识与决策行为的神经转向。最后指出认知地图空间分析的地理学在跨学科融合发展中的角色与应用前景。

外界环境中物体位置与空间关系在记忆中如何表征，一直是空间认知研究领域探讨和争论的热点问题。该文从空间表征的参照框架、朝向特异性、组织结构和存储内容四个方面，系统回顾了近年来对空间表征形成机制与内在特征的理论探讨。在此基础上，进一步讨论了当前空间表征研究中存在的生态效度问题，以及以后将虚拟环境技术引入到空间认知研究中的发展趋势

During realistic, continuous perception, humans automatically segment experiences into discrete events. Using a novel model of cortical event dynamics, we investigate how cortical structures generate event representations during narrative perception and how these events are stored to and retrieved from memory. Our data-driven approach allows us to detect event boundaries as shifts between stable patterns of brain activity without relying on stimulus annotations and reveals a nested hierarchy from short events in sensory regions to long events in high-order areas (including angular gyrus and posterior medial cortex), which represent abstract, multimodal situation models. High-order event boundaries are coupled to increases in hippocampal activity, which predict pattern reinstatement during later free recall. These areas also show evidence of anticipatory reinstatement as subjects listen to a familiar narrative. Based on these results, we propose that brain activity is naturally structured into nested events, which form the basis of long-term memory representations.Copyright © 2017 Elsevier Inc. All rights reserved.

Environmental boundaries anchor cognitive maps that support memory. However, trapezoidal boundary geometry distorts the regular firing patterns of entorhinal grid cells, proposedly providing a metric for cognitive maps. Here we test the impact of trapezoidal boundary geometry on human spatial memory using immersive virtual reality. Consistent with reduced regularity of grid patterns in rodents and a grid-cell model based on the eigenvectors of the successor representation, human positional memory was degraded in a trapezoid environment compared with a square environment-an effect that was particularly pronounced in the narrow part of the trapezoid. Congruent with changes in the spatial frequency of eigenvector grid patterns, distance estimates between remembered positions were persistently biased, revealing distorted memory maps that explained behaviour better than the objective maps. Our findings demonstrate that environmental geometry affects human spatial memory in a similar manner to rodent grid-cell activity and, therefore, strengthen the putative link between grid cells and behaviour along with their cognitive functions beyond navigation.

Anticipating the future is a key motif of the brain, possibly supported by mental simulation of upcoming events. Rodent single-cell recordings suggest the ability of spatially tuned cells to represent subsequent locations. Grid-like representations have been observed in the human entorhinal cortex during virtual and imagined navigation. However, hitherto it remains unknown if grid-like representations contribute to mental simulation in the absence of imagined movement. Participants imagined directions between building locations in a large-scale virtual-reality city while undergoing fMRI without re-exposure to the environment. Using multi-voxel pattern analysis, we provide evidence for representations of absolute imagined direction at a resolution of 30° in the parahippocampal gyrus, consistent with the head-direction system. Furthermore, we capitalize on the six-fold rotational symmetry of grid-cell firing to demonstrate a 60° periodic pattern-similarity structure in the entorhinal cortex. Our findings imply a role of the entorhinal grid-system in mental simulation and future thinking beyond spatial navigation.

The ability to anticipate and flexibly plan for the future is critical for achieving goal-directed outcomes. Extant data suggest that neural and cognitive stress mechanisms may disrupt memory retrieval and restrict prospective planning, with deleterious impacts on behavior. Here, we examined whether and how acute psychological stress influences goal-directed navigational planning and efficient, flexible behavior. Our methods combined fMRI, neuroendocrinology, and machine learning with a virtual navigation planning task. Human participants were trained to navigate familiar paths in virtual environments and then (concurrent with fMRI) performed a planning and navigation task that could be most efficiently solved by taking novel shortcut paths. Strikingly, relative to non-stressed control participants, participants who performed the planning task under experimentally induced acute psychological stress demonstrated (1) disrupted neural activity critical for mnemonic retrieval and mental simulation and (2) reduced traversal of shortcuts and greater reliance on familiar paths. These neural and behavioral changes under psychological stress were tied to evidence for disrupted neural replay of memory for future locations in the spatial environment, providing mechanistic insight into why and how stress can alter planning and foster inefficient behavior.Copyright © 2020 Elsevier Inc. All rights reserved.

Research in animals and humans has demonstrated that the hippocampus is critical for retrieving distinct representations of overlapping sequences of information. There is recent evidence that the caudate nucleus and orbitofrontal cortex are also involved in disambiguation of overlapping spatial representations. The hippocampus and caudate are functionally distinct regions, but both have anatomical links with the orbitofrontal cortex. The present study used an fMRI-based functional connectivity analysis in humans to examine the functional relationship between the hippocampus, caudate, and orbitofrontal cortex when participants use contextual information to navigate well-learned spatial routes which share common elements. Participants were trained outside the scanner to navigate virtual mazes from a first-person perspective. Overlapping condition mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping condition mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required contextual information identifying the current navigational route to guide the appropriate response for a given trial. Results revealed greater functional connectivity between the hippocampus, caudate, and orbitofrontal cortex for overlapping mazes compared to non-overlapping mazes. The current findings suggest that the hippocampus and caudate interact with prefrontal structures cooperatively for successful contextually dependent navigation.Copyright © 2012 Elsevier Inc. All rights reserved.

The ability to represent the world accurately relies on simultaneous coarse and fine-grained neural information coding, capturing both gist and detail of an experience. The longitudinal axis of the hippocampus may provide a gradient of representational granularity in spatial and episodic memory in rodents and humans [1-8]. Rodent place cells in the ventral hippocampus exhibit significantly larger place fields and greater autocorrelation than those in the dorsal hippocampus [1, 9-11], which may underlie a coarser and slower changing representation of space [10, 12]. Recent evidence suggests that properties of cellular dynamics in rodents can be captured with fMRI in humans during spatial navigation [13] and conceptual learning [14]. Similarly, mechanisms supporting granularity along the long axis may also be extrapolated to the scale of fMRI signal. Here, we provide the first evidence for separable scales of representation along the human hippocampal anteroposterior axis during navigation and rest by showing (1) greater similarity among voxel time courses and (2) higher temporal autocorrelation in anterior hippocampus (aHPC), relative to posterior hippocampus (pHPC), the human homologs of ventral and dorsal rodent hippocampus. aHPC voxels exhibited more similar activity at each time point and slower signal change over time than voxels in pHPC, consistent with place field organization in rodents. Importantly, similarity between voxels was related to navigational strategy and episodic memory. These findings provide evidence that the human hippocampus supports an anterior-to-posterior gradient of coarse-to-fine spatiotemporal representations, suggesting the existence of a cross-species mechanism, whereby lower neural similarity supports more complex coding of experience.Copyright © 2018 Elsevier Ltd. All rights reserved.

As we navigate the world, we use learned representations of relational structures to explore and to reach goals. Studies of how relational knowledge enables inference and planning are typically conducted in controlled small-scale settings. It remains unclear, however, how people use stored knowledge in continuously unfolding navigation (e.g., walking long distances in a city). We hypothesized that multiscale predictive representations guide naturalistic navigation in humans, and these scales are organized along posterior-anterior prefrontal and hippocampal hierarchies. We conducted model-based representational similarity analyses of neuroimaging data collected while male and female participants navigated realistically long paths in virtual reality. We tested the pattern similarity of each point, along each path, to a weighted sum of its successor points within predictive horizons of different scales. We found that anterior PFC showed the largest predictive horizons, posterior hippocampus the smallest, with the anterior hippocampus and orbitofrontal regions in between. Our findings offer novel insights into how cognitive maps support hierarchical planning at multiple scales.

Consistent patterns of errors are found in estimations of distances and angles along urban routes, even among subjects who know the areas well. These patterns can be used to discover the organization of the knowledge we use to find our way around in everyday life.

The firing patterns of grid cells in medial entorhinal cortex (mEC) and associated brain areas form triangular arrays that tessellate the environment [1, 2] and maintain constant spatial offsets to each other between environments [3, 4]. These cells are thought to provide an efficient metric for navigation in large-scale space [5-8]. However, an accurate and universal metric requires grid cell firing patterns to uniformly cover the space to be navigated, in contrast to recent demonstrations that environmental features such as boundaries can distort [9-11] and fragment [12] grid patterns. To establish whether grid firing is determined by local environmental cues, or provides a coherent global representation, we recorded mEC grid cells in rats foraging in an environment containing two perceptually identical compartments connected via a corridor. During initial exposures to the multicompartment environment, grid firing patterns were dominated by local environmental cues, replicating between the two compartments. However, with prolonged experience, grid cell firing patterns formed a single, continuous representation that spanned both compartments. Thus, we provide the first evidence that in a complex environment, grid cell firing can form the coherent global pattern necessary for them to act as a metric capable of supporting large-scale spatial navigation.Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.

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.

We use mental models of the world-cognitive maps-to guide behavior. The lateral orbitofrontal cortex (lOFC) is typically thought to support behavior by deploying these maps to simulate outcomes, but recent evidence suggests that it may instead support behavior by underlying map creation. We tested between these two alternatives using outcome-specific devaluation and a high-potency chemogenetic approach. Selectively inactivating lOFC principal neurons when male rats learned distinct cue-outcome associations, but before outcome devaluation, disrupted subsequent inference, confirming a role for the lOFC in creating new maps. However, lOFC inactivation surprisingly led to generalized devaluation, a result that is inconsistent with a complete mapping failure. Using a reinforcement learning framework, we show that this effect is best explained by a circumscribed deficit in credit assignment precision during map construction, suggesting that the lOFC has a selective role in defining the specificity of associations that comprise cognitive maps.© 2022. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

The role of the hippocampus in spatial cognition is incontrovertible yet controversial. Place cells, initially thought to be location-specifiers, turn out to respond promiscuously to a wide range of stimuli. Here we test the idea, which we have recently demonstrated in a computational model, that the hippocampal place cells may ultimately be interested in a space's topological qualities (its connectivity) more than its geometry (distances and angles); such higher-order functioning would be more consistent with other known hippocampal functions. We recorded place cell activity in rats exploring morphing linear tracks that allowed us to dissociate the geometry of the track from its topology. The resulting place fields preserved the relative sequence of places visited along the track but did not vary with the metrical features of the track or the direction of the rat's movement. These results suggest a reinterpretation of previous studies and new directions for future experiments.

A key component of spatial navigation is the ability to use visual information to ascertain where one is located and how one is oriented in the world. We used functional magnetic resonance imaging to examine the neural correlates of this phenomenon in humans. Subjects were scanned while retrieving different kinds of topographical and nontopographical information in response to visual scenes. In the three critical conditions, they viewed images of a familiar college campus, and reported either the location of the place depicted in the image (location task), the compass direction that the camera was facing when the image was taken (orientation task), or whether the location was on campus or not (familiarity task). Our analyses focused on the retrosplenial cortex (RSC)/parietal-occipital sulcus region and the parahippocampal place area (PPA), which previous studies indicate play a critical role in place recognition. RSC activity depended on the type of information retrieved, with the strongest response in the location task. In contrast, PPA activity did not depend on the retrieval task. Additional analyses revealed a strong effect of familiarity in RSC but not in the PPA, with the former region responding much more strongly to images of the familiar campus than to images of an unfamiliar campus. These results suggest that the PPA and RSC play distinct but complementary roles in place recognition. In particular, the PPA may primarily support perception of the immediate scene, whereas RSC may support memory retrieval mechanisms that allow the scene to be localized within the broader spatial environment.

The 'cognitive map' hypothesis proposes that brain builds a unified representation of the spatial environment to support memory and guide future action. Forty years of electrophysiological research in rodents suggest that cognitive maps are neurally instantiated by place, grid, border and head direction cells in the hippocampal formation and related structures. Here we review recent work that suggests a similar functional organization in the human brain and yields insights into how cognitive maps are used during spatial navigation. Specifically, these studies indicate that (i) the human hippocampus and entorhinal cortex support map-like spatial codes, (ii) posterior brain regions such as parahippocampal and retrosplenial cortices provide critical inputs that allow cognitive maps to be anchored to fixed environmental landmarks, and (iii) hippocampal and entorhinal spatial codes are used in conjunction with frontal lobe mechanisms to plan routes during navigation. We also discuss how these three basic elements of cognitive map based navigation-spatial coding, landmark anchoring and route planning-might be applied to nonspatial domains to provide the building blocks for many core elements of human thought.

Representing an environment globally, in a coarse way, and locally, in a fine-grained way, are two fundamental aspects of how our brain interprets the world that surrounds us. The neural correlates of these representations have not been explicated in humans. In this study we used fMRI to investigate these correlates and to explore a possible functional segregation in the hippocampus and parietal cortex. We hypothesized that processing a coarse, global environmental representation engages anterior parts of these regions, whereas processing fine-grained, local environmental information engages posterior parts. Participants learned a virtual environment and then had to find their way during fMRI. After scanning, we assessed strategies used and representations stored. Activation in the hippocampal head (anterior) was related to the multiple distance and global direction judgments and to the use of a coarse, global environmental representation during navigation. Activation in the hippocampal tail (posterior) was related to both local and global direction judgments and to using strategies like number of turns. A structural shape analysis showed that the use of a coarse, global environmental representation was related to larger right hippocampal head volume and smaller right hippocampal tail volume. In the inferior parietal cortex, a similar functional segregation was observed, with global routes represented anteriorly and fine-grained route information such as number of turns represented posteriorly. In conclusion, moving from the anterior to the posterior hippocampus and inferior parietal cortex reflects a shift from processing coarse global environmental representations to processing fine-grained, local environmental representations.

The brain forms cognitive maps of relational knowledge—an organizing principle thought to underlie our ability to generalize and make inferences. However, how can a relevant map be selected in situations where a stimulus is embedded in multiple relational structures? Here, we find that both spatial and predictive cognitive maps influence generalization in a choice task, where spatial location determines reward magnitude. Mirroring behavior, the hippocampus not only builds a map of spatial relationships but also encodes the experienced transition structure. As the task progresses, participants’ choices become more influenced by spatial relationships, reflected in a strengthening of the spatial map and a weakening of the predictive map. This change is driven by orbitofrontal cortex, which represents the degree to which an outcome is consistent with the spatial rather than the predictive map and updates hippocampal representations accordingly. Taken together, this demonstrates how hippocampal cognitive maps are used and updated flexibly for inference.

Cognitive maps are assumed to be fundamentally spatial and grounded only in perceptual processes, as supported by the discovery of functionally dedicated cell types in the human brain, which tile the environment in a maplike fashion. Challenging this view, we demonstrate that spatial representations-such as large-scale geographical maps-can be as well retrieved with high confidence from natural language through cognitively plausible artificial-intelligence models on the basis of nonspatial associative-learning mechanisms. More critically, we show that linguistic information accounts for the specific distortions observed in tasks when college-age adults have to judge the geographical positions of cities, even when these positions are estimated on real maps. These findings indicate that language experience can encode and reproduce cognitive maps without the need for a dedicated spatial-representation system, thus suggesting that the formation of these maps is the result of a strict interplay between spatial- and nonspatial-learning principles.

How animals navigate over large-scale environments remains a riddle. Specifically, it is debated whether animals have cognitive maps. The hallmark of map-based navigation is the ability to perform shortcuts, i.e., to move in direct but novel routes. When tracking an animal in the wild, it is extremely difficult to determine whether a movement is truly novel because the animal's past movement is unknown. We overcame this difficulty by continuously tracking wild fruit bat pups from their very first flight outdoors and over the first months of their lives. Bats performed truly original shortcuts, supporting the hypothesis that they can perform large-scale map-based navigation. We documented how young pups developed their visual-based map, exemplifying the importance of exploration and demonstrating interindividual differences.Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

Successful visual navigation requires a sense of the geometry of the local environment. How do our brains extract this information from retinal images? Here we visually presented scenes with all possible combinations of five scene-bounding elements (left, right, and back walls; ceiling; floor) to human subjects during functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG). The fMRI response patterns in the scene-responsive occipital place area (OPA) reflected scene layout with invariance to changes in surface texture. This result contrasted sharply with the primary visual cortex (V1), which reflected low-level image features of the stimuli, and the parahippocampal place area (PPA), which showed better texture than layout decoding. MEG indicated that the texture-invariant scene layout representation is computed from visual input within ∼100 ms, suggesting a rapid computational mechanism. Taken together, these results suggest that the cortical representation underlying our instant sense of the environmental geometry is located in the OPA.Copyright © 2019 Elsevier Inc. All rights reserved.

Despite decades of research on spatial memory, we know surprisingly little about how the brain guides navigation to goals. While some models argue that vectors are represented for navigational guidance, other models postulate that the future path is computed. Although the hippocampal formation has been implicated in processing spatial goal information, it remains unclear whether this region processes path- or vector-related information.We report neuroimaging data collected from subjects navigating London's Soho district; these data reveal that both the path distance and the Euclidean distance to the goal are encoded by the medial temporal lobe during navigation. While activity in the posterior hippocampus was sensitive to the distance along the path, activity in the entorhinal cortex was correlated with the Euclidean distance component of a vector to the goal. During travel periods, posterior hippocampal activity increased as the path to the goal became longer, but at decision points, activity in this region increased as the path to the goal became closer and more direct. Importantly, sensitivity to the distance was abolished in these brain areas when travel was guided by external cues.The results indicate that the hippocampal formation contains representations of both the Euclidean distance and the path distance to goals during navigation. These findings argue that the hippocampal formation houses a flexible guidance system that changes how it represents distance to the goal depending on the fluctuating demands of navigation.Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved.

Grid cells in the entorhinal cortex appear to represent spatial location via a triangular coordinate system. Such cells, which have been identified in rats, bats and monkeys, are believed to support a wide range of spatial behaviors. Recording neuronal activity from neurosurgical patients performing a virtual-navigation task, we identified cells exhibiting grid-like spiking patterns in the human brain, suggesting that humans and simpler animals rely on homologous spatial-coding schemes.

In the parallel map theory, the hippocampus encodes space with 2 mapping systems. The bearing map is constructed primarily in the dentate gyrus from directional cues such as stimulus gradients. The sketch map is constructed within the hippocampus proper from positional cues. The integrated map emerges when data from the bearing and sketch maps are combined. Because the component maps work in parallel, the impairment of one can reveal residual learning by the other. Such parallel function may explain paradoxes of spatial learning, such as learning after partial hippocampal lesions, taxonomic and sex differences in spatial learning, and the function of hippocampal neurogenesis. By integrating evidence from physiology to phylogeny, the parallel map theory offers a unified explanation for hippocampal function.

Central to the concept of the “cognitive map” is that it confers behavioral flexibility, allowing animals to take efficient detours, exploit shortcuts, and avoid alluring, but unhelpful, paths. The neural underpinnings of such naturalistic and flexible behavior remain unclear. In two neuroimaging experiments, we tested human participants on their ability to navigate to a set of goal locations in a virtual desert island riven by lava, which occasionally spread to block selected paths (necessitating detours) or receded to open new paths (affording real shortcuts or false shortcuts to be avoided). Detours activated a network of frontal regions compared with shortcuts. Activity in the right dorsolateral PFC specifically increased when participants encountered tempting false shortcuts that led along suboptimal paths that needed to be differentiated from real shortcuts. We also report modulation in event-related fields and theta power in these situations, providing insight to the temporal evolution of response to encountering detours and shortcuts. These results help inform current models as to how the brain supports navigation and planning in dynamic environments.

Thirty years of research suggests that environmental boundaries-e.g., the walls of an experimental chamber or room-exert powerful influence on navigational behavior, often to the exclusion of other cues [1-9]. Consistent with this behavioral work, neurons in brain structures that instantiate spatial memory often exhibit firing fields that are strongly controlled by environmental boundaries [10-15]. Despite the clear importance of environmental boundaries for spatial coding, however, a brain region that mediates the perception of boundary information has not yet been identified. We hypothesized that the occipital place area (OPA), a scene-selective region located near the transverse occipital sulcus [16], might provide this perceptual source by extracting boundary information from visual scenes during navigation. To test this idea, we used transcranial magnetic stimulation (TMS) to interrupt processing in the OPA while subjects performed a virtual-reality memory task that required them to learn the spatial locations of test objects that were either fixed in place relative to the boundary of the environment or moved in tandem with a landmark object. Consistent with our prediction, we found that TMS to the right OPA impaired spatial memory for boundary-tethered, but not landmark-tethered, objects. Moreover, this effect was found when the boundary was defined by a wall, but not when it was defined by a marking on the ground. These results show that the OPA is causally involved in boundary-based spatial navigation and suggest that the OPA is the perceptual source of the boundary information that controls navigational behavior.Copyright © 2016 Elsevier Ltd. All rights reserved.

In this paper, we review one of the oldest paradigms used in animal cognition: the detour paradigm. The paradigm presents the subject with a situation where a direct route to the goal is blocked and a detour must be made to reach it. Often being an ecologically valid and a versatile tool, the detour paradigm has been used to study diverse cognitive skills like insight, social learning, inhibitory control and route planning. Due to the relative ease of administrating detour tasks, the paradigm has lately been used in large-scale comparative studies in order to investigate the evolution of inhibitory control. Here we review the detour paradigm and some of its cognitive requirements, we identify various ecological and contextual factors that might affect detour performance, we also discuss developmental and neurological underpinnings of detour behaviors, and we suggest some methodological approaches to make species comparisons more robust.

Temporally organized reactivation of experiences during awake immobility periods is thought to underlie cognitive processes like planning and evaluation. While replay of trajectories is well established for the hippocampus, it is unclear whether the medial prefrontal cortex (mPFC) can reactivate sequential behavioral experiences in the awake state to support task execution. We simultaneously recorded from hippocampal and mPFC principal neurons in rats performing a mPFC-dependent rule-switching task on a plus maze. We found that mPFC neuronal activity encoded relative positions between the start and goal. During awake immobility periods, the mPFC replayed temporally organized sequences of these generalized positions, resembling entire spatial trajectories. The occurrence of mPFC trajectory replay positively correlated with rule-switching performance. However, hippocampal and mPFC trajectory replay occurred independently, indicating different functions. These results demonstrate that the mPFC can replay ordered activity patterns representing generalized locations and suggest that mPFC replay might have a role in flexible behavior. VIDEO ABSTRACT.Copyright © 2020 Elsevier Inc. All rights reserved.

The involvement of medial prefrontal cortex (mPFC) in spatial learning was examined in two memory tasks using spatial components, the Morris water maze and the three-panel runway. Using the Morris water maze task, with an invisible platform, the effects of NMDA mPFC lesions were assessed in a procedure reflecting spatial learning and memory, including a spatial reversal. In the three-panel runway, a delayed matching-to-position procedure was used in which rats were required to find food at the end of the runway after passing through one of three panel gates set into four barriers spaced equally apart along the maze. In addition, mPFC lesions were assessed behaviorally in two behavioral tests known to be sensitive to mPFC dysfunction: the food hoarding paradigm and spontaneous locomotion in the open field. Consistent with the documented effects of mPFC damage, NMDA mPFC lesions impaired food hoarding behavior and increased spontaneous exploratory locomotion. In the Morris water maze and the three-panel runway, mPFC-lesioned rats showed relatively few effects, supporting the conclusion that the damage inflicted to the mPFC had no consequence for the processing of spatial information. However, mPFC lesioned animals showed slower acquisition during both the training trial in the three-panel runway and the reversal training in the Morris water maze. These results suggest that spatial memory did not depend on mPFC integrity in the Morris water maze and the three-panel runway experiments, and address the issue of deficits induced by mPFC lesions in memory tasks dependent on non-mnemonic processes such as attentional processes and/or a reduced behavioral flexibility to environmental changes.

"Boundary vector cells" were predicted to exist by computational models of the environmental inputs underlying the spatial firing patterns of hippocampal place cells (O'Keefe and Burgess, 1996; Burgess et al., 2000; Hartley et al., 2000). Here, we report the existence of cells fulfilling this description in recordings from the subiculum of freely moving rats. These cells may contribute environmental information to place cell firing, complementing path integrative information. Their relationship to other cell types, including medial entorhinal "border cells," is discussed.

Our body is central to our sense of self, and distorted body representations are found in several serious medical conditions. This paper reviews evidence that distortions of body representations are also common in healthy individuals, and occur in domains including tactile spatial perception, proprioception, and the conscious body image. Across domains, there is a general tendency for body width to be overestimated compared to body length. Intriguingly, distortions in both eating disorders and chronic pain appear to be exaggerations of this baseline pattern of distortions, suggesting that these conditions may relate to dysfunction of mechanisms for body perception. Distortions of body representations provide a revealing window into basic aspects of self-perception.Copyright © 2021 Elsevier Ltd. All rights reserved.

The use of landmarks is central to many navigational strategies. Here we use multivoxel pattern analysis of fMRI data to understand how landmarks are coded in the human brain. Subjects were scanned while viewing the interiors and exteriors of campus buildings. Despite their visual dissimilarity, interiors and exteriors corresponding to the same building elicited similar activity patterns in the parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area (OPA), three regions known to respond strongly to scenes and buildings. Generalization across stimuli depended on knowing the correspondences among them in the PPA but not in the other two regions, suggesting that the PPA is the key region involved in learning the different perceptual instantiations of a landmark. In contrast, generalization depended on the ability to freely retrieve information from memory in RSC, and it did not depend on familiarity or cognitive task in OPA. Together, these results suggest a tripartite division of labor, whereby PPA codes landmark identity, RSC retrieves spatial or conceptual information associated with landmarks, and OPA processes visual features that are important for landmark recognition.A central element of spatial navigation is the ability to recognize the landmarks that mark different places in the world. However, little is known about how the brain performs this function. Here we show that the parahippocampal place area (PPA), a region in human occipitotemporal cortex, exhibits key features of a landmark recognition mechanism. Specifically, the PPA treats different perceptual instantiations of the same landmark as representationally similar, but only when subjects have enough experience to know the correspondences among the stimuli. We also identify two other brain regions that exhibit landmark generalization, but with less sensitivity to familiarity. These results elucidate the brain networks involved in the learning and recognition of navigational landmarks.Copyright © 2015 the authors 0270-6474/15/3514896-13$15.00/0.

Two classes of space define our everyday experience within our surrounding environment: vista spaces, such as rooms or streets which can be perceived from one vantage point, and environmental spaces, for example, buildings and towns which are grasped from multiple views acquired during locomotion. However, theories of spatial representations often treat both spaces as equal. The present experiments show that this assumption cannot be upheld. Participants learned exactly the same layout of objects either within a single room or spread across multiple corridors. By utilizing a pointing and a placement task we tested the acquired configurational memory. In Experiment 1 retrieving memory of the object layout acquired in environmental space was affected by the distance of the traveled path and the order in which the objects were learned. In contrast, memory retrieval of objects learned in vista space was not bound to distance and relied on different ordering schemes (e.g., along the layout structure). Furthermore, spatial memory of both spaces differed with respect to the employed reference frame orientation. Environmental space memory was organized along the learning experience rather than layout intrinsic structure. In Experiment 2 participants memorized the object layout presented within the vista space room of Experiment 1 while the learning procedure emulated environmental space learning (movement, successive object presentation). Neither factor rendered similar results as found in environmental space learning. This shows that memory differences between vista and environmental space originated mainly from the spatial compartmentalization which was unique to environmental space learning. Our results suggest that transferring conclusions from findings obtained in vista space to environmental spaces and vice versa should be made with caution.Copyright © 2016 Elsevier B.V. All rights reserved.

Two experiments examined the acquisition of cognitive maps of two intersecting routes through an urban area. In the presentation stage of the experiments, slides of the two routes were shown in order to simulate travel along the routes. The number of presentations of the slides was varied. In the test stage, subjects made directional and distance judgements from memory between places on the routes. The results suggest that from the start of acquisition of the spatial layout of the routes, subjects used network schemata in which both routes were combined, rather than a separate scheme for each route which were later combined. During initial acquisitions of the routes, a direction of travel bias was found such that spatial judgements from memory tended to be more accurate in the direction of travel along the routes than in the opposite direction. The findings imply that, at least during early acquisition, the spatial properties of the routes were encoded in terms of sequential associations.

Spatial navigation is believed to be guided in part by reference to an internal map of the environment. We used functional magnetic resonance imaging (fMRI) to test for a key aspect of a cognitive map: preservation of real-world distance relationships. University students were scanned while viewing photographs of familiar campus landmarks. fMRI response levels in the left hippocampus corresponded to real-world distances between landmarks shown on successive trials, indicating that this region considered closer landmarks to be more representationally similar and more distant landmarks to be more representationally distinct. In contrast, posterior visually responsive regions such as retrosplenial complex and the parahippocampal place area were sensitive to landmark repetition and encoded landmark identity in their multivoxel activity patterns but did not show a distance-related response. These data suggest the existence of a map-like representation in the human medial temporal lobe that encodes the coordinates of familiar locations in large-scale, real-world environments.

More than three decades of research have demonstrated a role for hippocampal place cells in representation of the spatial environment in the brain. New studies have shown that place cells are part of a broader circuit for dynamic representation of self-location. A key component of this network is the entorhinal grid cells, which, by virtue of their tessellating firing fields, may provide the elements of a path integration-based neural map. Here we review how place cells and grid cells may form the basis for quantitative spatiotemporal representation of places, routes, and associated experiences during behavior and in memory. Because these cell types have some of the most conspicuous behavioral correlates among neurons in nonsensory cortical systems, and because their spatial firing structure reflects computations internally in the system, studies of entorhinal-hippocampal representations may offer considerable insight into general principles of cortical network dynamics.

For visually guided navigation, the use of environmental cues is essential. Particularly, detecting local boundaries that impose limits to locomotion and estimating their location is crucial. In a series of three fMRI experiments, we investigated whether there is a neural coding of navigational distance in the human visual cortex (both female and male). We used virtual reality software to systematically manipulate the distance from a viewer perspective to different types of a boundary. Using a multivoxel pattern classification employing a linear support vector machine, we found that the occipital place area (OPA) is sensitive to the navigational distance restricted by the transparent glass wall. Further, the OPA was sensitive to a non-crossable boundary only, suggesting an importance of the functional constraint of a boundary. Together, we propose the OPA as a perceptual source of external environmental features relevant for navigation. One of major goals in cognitive neuroscience has been to understand the nature of visual scene representation in human ventral visual cortex. An aspect of scene perception that has been overlooked despite its ecological importance is the analysis of space for navigation. One of critical computation necessary for navigation is coding of distance to environmental boundaries that impose limit on navigator's movements. This paper reports the first empirical evidence for coding of navigational distance in the human visual cortex and its striking sensitivity to functional constraint of environmental boundaries. Such finding links the paper to previous neurological and behavioral works that emphasized the distance to boundaries as a crucial geometric property for reorientation behavior of children and other animal species.Copyright © 2020 the authors.

Generalizing experiences to guide decision-making in novel situations is a hallmark of flexible behavior. Cognitive maps of an environment or task can theoretically afford such flexibility, but direct evidence has proven elusive. In this study, we found that discretely sampled abstract relationships between entities in an unseen two-dimensional social hierarchy are reconstructed into a unitary two-dimensional cognitive map in the hippocampus and entorhinal cortex. We further show that humans use a grid-like code in entorhinal cortex and medial prefrontal cortex for inferred direct trajectories between entities in the reconstructed abstract space during discrete decisions. These grid-like representations in the entorhinal cortex are associated with decision value computations in the medial prefrontal cortex and temporoparietal junction. Collectively, these findings show that grid-like representations are used by the human brain to infer novel solutions, even in abstract and discrete problems, and suggest a general mechanism underpinning flexible decision-making and generalization.© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.

Cognitive maps enable efficient inferences from limited experience that can guide novel decisions. We tested whether the hippocampus (HC), entorhinal cortex (EC), and ventromedial prefrontal cortex (vmPFC)/medial orbitofrontal cortex (mOFC) organize abstract and discrete relational information into a cognitive map to guide novel inferences. Subjects learned the status of people in two unseen 2D social hierarchies, with each dimension learned on a separate day. Although one dimension was behaviorally relevant, multivariate activity patterns in HC, EC, and vmPFC/mOFC were linearly related to the Euclidean distance between people in the mentally reconstructed 2D space. Hubs created unique comparisons between the hierarchies, enabling inferences between novel pairs. We found that both behavior and neural activity in EC and vmPFC/mOFC reflected the Euclidean distance to the retrieved hub, which was reinstated in HC. These findings reveal how abstract and discrete relational structures are represented, are combined, and enable novel inferences in the human brain.Copyright © 2020 Elsevier Inc. All rights reserved.

The prefrontal cortex (PFC) supports decision-making, goal tracking, and planning. Spatial navigation is a behavior that taxes these cognitive processes, yet the role of the PFC in models of navigation has been largely overlooked. In humans, activity in dorsolateral PFC (dlPFC) and ventrolateral PFC (vlPFC) during detours, reveal a role in inhibition and replanning. Dorsal anterior cingulate cortex (dACC) is implicated in planning and spontaneous internally-generated changes of route. Orbitofrontal cortex (OFC) integrates representations of the environment with the value of actions, providing a 'map' of possible decisions. In rodents, medial frontal areas interact with hippocampus during spatial decisions and switching between navigation strategies. In reviewing these advances, we provide a framework for how different prefrontal regions may contribute to different stages of navigation.Copyright © 2021 Elsevier Ltd. All rights reserved.

Humans and animals use mental representations of the spatial structure of the world to navigate. The classical view is that these representations take the form of Euclidean cognitive maps, but alternative theories suggest that they are cognitive graphs consisting of locations connected by paths. We review evidence suggesting that both map-like and graph-like representations exist in the mind/brain that rely on partially overlapping neural systems. Maps and graphs can operate simultaneously or separately, and they may be applied to both spatial and nonspatial knowledge. By providing structural frameworks for complex information, cognitive maps and cognitive graphs may provide fundamental organizing schemata that allow us to navigate in physical, social, and conceptual spaces.Copyright © 2020 Elsevier Ltd. All rights reserved.

There is evidence that wild animals are able to recall key locations and associate them with navigational routes. Studies in primate navigation suggest most species navigate through the route network system, using intersections among routes as locations of decision-making. Recent approaches presume that points of directional change may be key locations where animals decide where to go next. Over four consecutive years, we observed how a wild group of bearded capuchin monkeys used a route network system and Change Point locations (CPs) in the Brazilian ecotone of Cerrado-Caatinga. We built 200 daily routes of one wild bearded capuchin group. We used ArcGIS, the Change Point Test, Spatial Analysis in Macroecology (SAM), and statistical models to test the hypothesis that wild bearded capuchins use CPs located along routes in a different fashion than they use the CPs located at intersections of routes. A logistic regression model was used to determine the landscape variables affecting capuchins' directional changes at intersections or along routes. CPs at intersections were important points of travel path changes, whereas CPs along routes represented a zig-zag movement along the routes following the landscape features. CPs at intersections were associated with steeper terrains and shorter distances from important resources, along with better visibility of the home range. Our results support the hypothesis that intersections among routes in the route network system are located at points where monkeys have the best visibility available to make decisions on where to visit next.

We experience our visual environment as a seamless, immersive panorama. Yet, each view is discrete and fleeting, separated by expansive eye movements and discontinuous views of our spatial surroundings. How are discrete views of a panoramic environment knit together into a broad, unified memory representation? Regions of the brain's "scene network" are well poised to integrate retinal input and memory [1]: they are visually driven [2, 3] but also densely interconnected with memory structures in the medial temporal lobe [4]. Further, these regions harbor memory signals relevant for navigation [5-8] and adapt across overlapping shifts in scene viewpoint [9, 10]. However, it is unknown whether regions of the scene network support visual memory for the panoramic environment outside of the current field of view and, further, how memory for the surrounding environment influences ongoing perception. Here, we demonstrate that specific regions of the scene network-the retrosplenial complex (RSC) and occipital place area (OPA)-unite discrete views of a 360° panoramic environment, both current and out of sight, in a common representational space. Further, individual scene views prime associated representations of the panoramic environment in behavior, facilitating subsequent perceptual judgments. We propose that this dynamic interplay between memory and perception plays an important role in weaving the fabric of continuous visual experience.Copyright © 2016 Elsevier Ltd. All rights reserved.

Cognitive maps are encoded in the hippocampal formation and related regions and range from the spatial to the purely conceptual. Neural mechanisms that encode information into relational structures, up to an arbitrary level of abstraction, may explain such a broad range of representation. Research now indicates that social life can also be mapped by these mechanisms: others' spatial locations, social memory, and even a two-dimensional social space framed by social power and affiliation. The systematic mapping of social life onto a relational social space facilitates adaptive social decision making, akin to social navigation. This emerging line of research has implications for cognitive mapping research, clinical disorders that feature hippocampal dysfunction, and the field of social cognitive neuroscience.Copyright © 2018 Elsevier Inc. All rights reserved.

Classical theories of spatial microgenesis (Siegel and White, 1975) posit that information about landmarks and the paths between them is acquired prior to the establishment of more holistic survey-level representations. To test this idea, we examined the neural and behavioral correlates of landmark and path encoding during a real-world route learning episode. Subjects were taught a novel 3 km route around the University of Pennsylvania campus and then brought to the laboratory where they performed a recognition task that required them to discriminate between on-route and off-route buildings. Each building was preceded by a masked prime, which could either be the building that immediately preceded the target building along the route or immediately succeeded it. Consistent with previous reports using a similar paradigm in a virtual environment (Janzen and Weststeijn, 2007), buildings at navigational decision points (DPs) were more easily recognized than non-DP buildings and recognition was facilitated by in-route vs. against-route primes. Functional magnetic resonance imaging (fMRI) data collected during the recognition task revealed two effects of interest: first, greater response to DP vs. non-DP buildings in a wide network of brain regions previously implicated in spatial processing; second, a significant interaction between building location (DP vs. non-DP) and route direction (in-route vs. against-route) in a retrosplenial/parietal-occipital sulcus region previously labeled the retrosplenial complex (RSC). These results indicate that newly learned real-world routes are coded in terms of paths between decision points and suggest that the RSC may be a critical locus for integrating landmark and path information.Copyright 2010 Elsevier Inc. All rights reserved.

The high storage capacity of the episodic memory system relies on distinct representations for events that are separated in time and space. The spatial component of these computations includes the formation of independent maps by hippocampal place cells across environments, referred to as global remapping. Such remapping is thought to emerge by the switching of input patterns from specialized spatially selective cells in medial entorhinal cortex (mEC), such as grid and border cells. Although it has been shown that acute manipulations of mEC firing patterns are sufficient for inducing hippocampal remapping, it remains unknown whether specialized spatial mEC inputs are necessary for the reorganization of hippocampal spatial representations. Here, we examined remapping in rats without mEC input to the hippocampus and found that highly distinct spatial maps emerged rapidly in every individual rat. Our data suggest that hippocampal spatial computations do not depend on inputs from specialized cell types in mEC.Copyright © 2018 The Author(s). Published by Elsevier Inc. All rights reserved.

Although the orbitofrontal cortex (OFC) has been studied intensely for decades, its precise functions have remained elusive. We recently hypothesized that the OFC contains a "cognitive map" of task space in which the current state of the task is represented, and this representation is especially critical for behavior when states are unobservable from sensory input. To test this idea, we apply pattern-classification techniques to neuroimaging data from humans performing a decision-making task with 16 states. We show that unobservable task states can be decoded from activity in OFC, and decoding accuracy is related to task performance and the occurrence of individual behavioral errors. Moreover, similarity between the neural representations of consecutive states correlates with behavioral accuracy in corresponding state transitions. These results support the idea that OFC represents a cognitive map of task space and establish the feasibility of decoding state representations in humans using non-invasive neuroimaging. Copyright © 2016 Elsevier Inc. All rights reserved.

The hippocampus and prefrontal cortex have both been implicated in various aspects of the acquisition, retention and performance of delayed matching to position (DMTP) tasks in the rat, although their precise respective contributions remain unclear. In the present study, rats were trained preoperatively on DMTP before receiving excitotoxic bilateral lesions of either the entire hippocampus or the medial prefrontal cortex. Rats with lesions of the prefrontal cortex exhibited a significant delay-dependent impairment on retention of the DMTP task, whereas hippocampal lesions were without effect. Rats were also exposed to a switch in the contingencies to a 'non-matching' rule, as an analogue of switching between decision rules in the human Wisconsin Card Sorting Test, in which human patients with prefrontal damage are impaired. Both lesion groups acquired the new contingency at control levels, providing no evidence towards a role for either of these areas in this type of rule-switching. The same rats were also assessed in a spatial reference memory task in the water maze, which revealed an impairment in escape latencies and path length that was specific to the hippocampal lesions. The results corroborate previous evidence that the hippocampus is not necessary for at least some aspects of working memory performance in the DMTP task, whereas the delay-dependent deficit in the prefrontal lesion group support this task as a potentially powerful tool for assessing the cognitive changes associated with frontal damage and repair.

A cognitive map has long been the dominant metaphor for hippocampal function, embracing the idea that place cells encode a geometric representation of space. However, evidence for predictive coding, reward sensitivity and policy dependence in place cells suggests that the representation is not purely spatial. We approach this puzzle from a reinforcement learning perspective: what kind of spatial representation is most useful for maximizing future reward? We show that the answer takes the form of a predictive representation. This representation captures many aspects of place cell responses that fall outside the traditional view of a cognitive map. Furthermore, we argue that entorhinal grid cells encode a low-dimensionality basis set for the predictive representation, useful for suppressing noise in predictions and extracting multiscale structure for hierarchical planning.

The term “cognitive template” originated from work in human-based cognitive science to describe a literal, stored, neural representation used in recognition tasks. As the study of cognition has expanded to nonhuman animals, the term has diffused to describe a wider range of animal cognitive tools and strategies that guide action through the recognition of and discrimination between external states. One potential reason for this nonstandardized meaning and variable employment is that researchers interested in the broad range of animal recognition tasks enjoy the simplicity of the cognitive template concept and have allowed it to become shorthand for many dissimilar or unknown neural processes without deep scrutiny of how this metaphor might comport with underlying neurophysiology. We review the functional evidence for cognitive templates in fields such as perception, navigation, communication, and learning, highlighting any neural correlates identified by these studies. We find that the concept of cognitive templates has facilitated valuable exploration at the interface between animal behavior and cognition, but the quest for a literal template has failed to attain mechanistic support at the level of neurophysiology. This may be the result of a misled search for a single physical locus for the “template” itself. We argue that recognition and discrimination processes are best treated as emergent and, as such, may not be physically localized within single structures of the brain. Rather, current evidence suggests that such tasks are accomplished through synergies between multiple distributed processes in animal nervous systems. We thus advocate for researchers to move toward a more ecological, process-oriented conception, especially when discussing the neural underpinnings of recognition-based cognitive tasks.

This paper is a study of the behavioral and spatial firing correlates of neurons in the rat postsubiculum. Recordings were made from postsubicular neurons as rats moved freely throughout a cylindrical chamber, where the major cue for orientation was a white card taped to the inside wall. An automatic video/computer system monitored cell discharge while simultaneously tracking the position of 2 colored light emitting diodes (LEDs) secured to the animal's head. The animal's location was calculated from the position of one of the LEDs and head direction in the horizontal plane calculated from the relative positions of the 2 LEDs. Approximately 26% of the cells were classified as head-direction cells because they discharged as a function of the animal's head direction in the horizontal plane, independent of the animal's behavior, location, or trunk position. For each head-direction cell, vectors drawn in the direction of maximal firing were parallel throughout the recording chamber and did not converge toward a single point. Plots of firing rate versus head direction showed that each firing-rate/head-direction function was adequately described by a triangular function. Each cell's maximum firing rate occurred at only one (the preferred) head direction; firing rates at head directions on either side of the preferred direction decreased linearly with angular deviation from the preferred direction. Results from 24 head-direction cells in 7 animals showed an equal distribution of preferred firing directions over a 360 degrees angle. The peak firing rate of head-direction cells varied from 5 to 115 spikes/sec (mean: 35). The range of head-direction angles over which discharge was elevated (directional firing range) was usually about 90 degrees, with little, if any, discharge at head directions outside this range. Quantitative analysis showed the location of the animal within the cylinder had minimal effect on directional cell firing. For each head-direction cell, the preferred direction, peak firing rate, and directional firing range remained stable for days. These results identify a new cell type that signals the animal's head direction in its environment.

Humans and other animals build up spatial knowledge of the environment on the basis of visual information and path integration. We compare three hypotheses about the geometry of this knowledge of navigation space: (a) 'cognitive map' with metric Euclidean structure and a consistent coordinate system, (b) 'topological graph' or network of paths between places, and (c) 'labelled graph' incorporating local metric information about path lengths and junction angles. In two experiments, participants walked in a non-Euclidean environment, a virtual hedge maze containing two 'wormholes' that visually rotated and teleported them between locations. During training, they learned the metric locations of eight target objects from a 'home' location, which were visible individually. During testing, shorter wormhole routes to a target were preferred, and novel shortcuts were directional, contrary to the topological hypothesis. Shortcuts were strongly biased by the wormholes, with mean constant errors of 37° and 41° (45° expected), revealing violations of the metric postulates in spatial knowledge. In addition, shortcuts to targets near wormholes shifted relative to flanking targets, revealing 'rips' (86% of cases), 'folds' (91%), and ordinal reversals (66%) in spatial knowledge. Moreover, participants were completely unaware of these geometric inconsistencies, reflecting a surprising insensitivity to Euclidean structure. The probability of the shortcut data under the Euclidean map model and labelled graph model indicated decisive support for the latter (BF>100). We conclude that knowledge of navigation space is best characterized by a labelled graph, in which local metric information is approximate, geometrically inconsistent, and not embedded in a common coordinate system. This class of 'cognitive graph' models supports route finding, novel detours, and rough shortcuts, and has the potential to unify a range of data on spatial navigation.Copyright © 2017 Elsevier B.V. All rights reserved.

Natural environments are represented by local maps of grid cells and place cells that are stitched together. The manner by which transitions between map fragments are generated is unknown. We recorded grid cells while rats were trained in two rectangular compartments, A and B (each 1 m × 2 m), separated by a wall. Once distinct grid maps were established in each environment, we removed the partition and allowed the rat to explore the merged environment (2 m × 2 m). The grid patterns were largely retained along the distal walls of the box. Nearer the former partition line, individual grid fields changed location, resulting almost immediately in local spatial periodicity and continuity between the two original maps. Grid cells belonging to the same grid module retained phase relationships during the transformation. Thus, when environments are merged, grid fields reorganize rapidly to establish spatial periodicity in the area where the environments meet.

The hippocampal-entorhinal system is important for spatial and relational memory tasks. We formally link these domains, provide a mechanistic understanding of the hippocampal role in generalization, and offer unifying principles underlying many entorhinal and hippocampal cell types. We propose medial entorhinal cells form a basis describing structural knowledge, and hippocampal cells link this basis with sensory representations. Adopting these principles, we introduce the Tolman-Eichenbaum machine (TEM). After learning, TEM entorhinal cells display diverse properties resembling apparently bespoke spatial responses, such as grid, band, border, and object-vector cells. TEM hippocampal cells include place and landmark cells that remap between environments. Crucially, TEM also aligns with empirically recorded representations in complex non-spatial tasks. TEM also generates predictions that hippocampal remapping is not random as previously believed; rather, structural knowledge is preserved across environments. We confirm this structural transfer over remapping in simultaneously recorded place and grid cells.Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Flexibility is a hallmark of memories that depend on the hippocampus. For navigating animals, flexibility is necessitated by environmental changes such as blocked paths and extinguished food sources. To better understand the neural basis of this flexibility, we recorded hippocampal replays in a spatial memory task where barriers as well as goals were moved between sessions to see whether replays could adapt to new spatial and reward contingencies. Strikingly, replays consistently depicted new goal-directed trajectories around each new barrier configuration and largely avoided barrier violations. Barrier-respecting replays were learned rapidly and did not rely on place cell remapping. These data distinguish sharply between place field responses, which were largely stable and remained tied to sensory cues, and replays, which changed flexibly to reflect the learned contingencies in the environment and suggest sequenced activations such as replay to be an important link between the hippocampus and flexible memory.Copyright © 2022. Published by Elsevier Inc.

Hippocampal place-cell replay has been proposed as a fundamental mechanism of learning and memory, which might support navigational learning and planning. An important hypothesis of relevance to these proposed functions is that the information encoded in replay should reflect the topological structure of experienced environments; that is, which places in the environment are connected with which others. Here we report several attributes of replay observed in rats exploring a novel forked environment that support the hypothesis. First, we observed that overlapping replays depicting divergent trajectories through the fork recruited the same population of cells with the same firing rates to represent the common portion of the trajectories. Second, replay tended to be directional and to flip the represented direction at the fork. Third, replay-associated sharp-wave-ripple events in the local field potential exhibited substructure that mapped onto the maze topology. Thus, the spatial complexity of our recording environment was accurately captured by replay: the underlying neuronal activities reflected the bifurcating shape, and both directionality and associated ripple structure reflected the segmentation of the maze. Finally, we observed that replays occurred rapidly after small numbers of experiences. Our results suggest that hippocampal replay captures learned information about environmental topology to support a role in navigation.

Mental representations are the essence of cognition. Yet to understand how the mind works, one must understand not just the content of mental representations (i.e., what information is stored) but also the format of those representations (i.e., how that information is stored). But what does it mean for representations to be formatted? How many formats are there? Is it possible that the mind represents some pieces of information in multiple formats at once? To address these questions, I discuss a “case study” of representational format: the representation of spatial location. I review work (a) across species and across development, (b) across spatial scales, and (c) across levels of analysis (e.g., high-level cognitive format vs. low-level neural format). Along the way, I discuss the possibility that the same information may be organized in multiple formats simultaneously (e.g., that locations may be represented in both Cartesian and polar coordinates). Ultimately, I argue that seemingly “redundant” formats may support the flexible spatial behavior observed in humans and that researchers should approach the study of all mental representations with this possibility in mind.

A cognitive map, representing an environment around oneself, is necessary for spatial navigation. However, compared with its constituent elements such as individual landmarks, neural substrates of coherent spatial information, which consists in a relationship among the individual elements, remain largely unknown. The present study investigated how the brain codes map-like representations in a virtual environment specified by the relative positions of three objects. Representational similarity analysis revealed an object-based spatial representation in the hippocampus (HPC) when participants located themselves within the environment, while the medial prefrontal cortex (mPFC) represented it when they recollected a target object’s location relative to their self-body. During recollection, task-dependent functional connectivity increased between the two areas implying exchange of self-location and target location signals between the HPC and mPFC. Together, the object-based cognitive map, whose coherent spatial information could be formed by objects, may be recruited in the HPC and mPFC for complementary functions during navigation, which may generalize to other aspects of cognition, such as navigating social interactions.

Individuals use social information to guide social interactions and to update relationships along multiple social dimensions. However, it is unclear what neural basis underlies this process of abstract "social navigation". In the current study, we recruited twenty-nine participants who performed a choose-your-own-adventure game in which they interacted with fictional characters during fMRI scanning. Using a whole-brain GLM approach, we found that vectors encoding two-dimensional information about the relationships predicted BOLD responses in the hippocampus and the precuneus, replicating previous work. We also explored whether these geometric representations were related to key brain regions previously identified in physical and abstract spatial navigation studies, but we did not find involvement of the entorhinal cortex, parahippocampal gyrus or the retrosplenial cortex. Finally, we used psychophysiological interaction analysis and identified a network of regions that correlated during participants' decisions, including the left posterior hippocampus, precuneus, dorsolateral prefrontal cortex (dlPFC), and the insula. Our findings suggest a brain network for social navigation in multiple abstract, social dimensions that includes the hippocampus, precuneus, dlPFC, and insula.© 2022. The Author(s).

Studies of human and rodent navigation often reveal a remarkable cross-species similarity between the cognitive and neural mechanisms of navigation. Such cross-species resemblance often overshadows some critical differences between how humans and nonhuman animals navigate. In this review, I propose that a navigation system requires both a storage system (i.e., representing spatial information) and a positioning system (i.e., sensing spatial information) to operate. I then argue that the way humans represent spatial information is different from that inferred from the cellular activity observed during rodent navigation. Such difference spans the whole hierarchy of spatial representation, from representing the structure of an environment to the representation of subregions of an environment, routes and paths, and the distance and direction relative to a goal location. These cross-species inconsistencies suggest that what we learn from rodent navigation does not always transfer to human navigation. Finally, I argue for closing the loop for the dominant, unidirectional animal-to-human approach in navigation research so that insights from behavioral studies of human navigation may also flow back to shed light on the cellular mechanisms of navigation for both humans and other mammals (i.e., a human-to-animal approach).