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• W2890141662 abstract "The ability to recover one’s bearings when lost is a skill that is fundamental for spatial navigation. We review the cognitive and neural mechanisms that underlie this ability, with the aim of linking together previously disparate findings from animal behavior, human psychology, electrophysiology, and cognitive neuroscience. Behavioral work suggests that reorientation involves two key abilities: first, the recovery of a spatial reference frame (a cognitive map) that is appropriate to the current environment; and second, the determination of one’s heading and location relative to that reference frame. Electrophysiological recording studies, primarily in rodents, have revealed potential correlates of these operations in place, grid, border/boundary, and head-direction cells in the hippocampal formation. Cognitive neuroscience studies, primarily in humans, suggest that the perceptual inputs necessary for these operations are processed by neocortical regions such as the retrosplenial complex, occipital place area and parahippocampal place area, with the retrosplenial complex mediating spatial transformations between the local environment and the recovered spatial reference frame, the occipital place area supporting perception of local boundaries, and the parahippocampal place area processing visual information that is essential for identification of the local spatial context. By combining results across these various literatures, we converge on a unified account of reorientation that bridges the cognitive and neural domains. The ability to recover one’s bearings when lost is a skill that is fundamental for spatial navigation. We review the cognitive and neural mechanisms that underlie this ability, with the aim of linking together previously disparate findings from animal behavior, human psychology, electrophysiology, and cognitive neuroscience. Behavioral work suggests that reorientation involves two key abilities: first, the recovery of a spatial reference frame (a cognitive map) that is appropriate to the current environment; and second, the determination of one’s heading and location relative to that reference frame. Electrophysiological recording studies, primarily in rodents, have revealed potential correlates of these operations in place, grid, border/boundary, and head-direction cells in the hippocampal formation. Cognitive neuroscience studies, primarily in humans, suggest that the perceptual inputs necessary for these operations are processed by neocortical regions such as the retrosplenial complex, occipital place area and parahippocampal place area, with the retrosplenial complex mediating spatial transformations between the local environment and the recovered spatial reference frame, the occipital place area supporting perception of local boundaries, and the parahippocampal place area processing visual information that is essential for identification of the local spatial context. By combining results across these various literatures, we converge on a unified account of reorientation that bridges the cognitive and neural domains. At some point in our lives, all of us have had the unsettling experience of losing our spatial bearings. Perhaps we had come up from a subway station onto a busy street and did not know which way we were facing. Perhaps we had taken a walk in the woods and lost track of where we were. In situations like these, unless we are aided by another person or a navigational device such as a compass or global positioning system, we must look out at the world and use perceptual information to figure out where we are and which way we are facing. In other words, we must spatially reorient ourselves. How do we accomplish this? And what are the neural systems involved? The experience of being lost underscores the fact that we are spatially oriented much of the time — but not always. This psychological distinction between orientation and disorientation implies the existence of an internal representation of large-scale navigable space that we use to keep track of our current spatial situation. Such a representation is referred to as a cognitive map. In its strongest form, a cognitive map could be a Euclidean coordinate system [1O’Keefe J. Nadel L. The Hippocampus as a Cognitive Map. Clarendon Press Oxford, 1978Google Scholar, 2Gallistel C.R. The Organization of Learning. The MIT Press, 1990Google Scholar], although less rigid forms of spatial knowledge, such as graph-like representations [3Trullier O. Wiener S.I. Berthoz A. Meyer J.A. Biologically based artificial navigation systems: Review and prospects.Prog. Neurobiol. 1997; 51: 483-544Crossref PubMed Scopus (0) Google Scholar, 4Kuipers B. The spatial semantic hierarchy. Artif.Intell. 2000; 119: 191-233Google Scholar, 5Chrastil E.R. Warren W.H. From cognitive maps to cognitive graphs.PloS One. 2014; 9: e112544Crossref PubMed Scopus (17) Google Scholar], are also possible. When we are disoriented, we no longer know where we are or which way we are facing on the map, and when we are misoriented, we have plotted our map location or heading inaccurately. There are two ways that an oriented navigator can update their map coordinates as they move around the world. Path integration, sometimes called dead reckoning, involves the use of idiothetic cues, such as vestibular information, motor efference copies, proprioceptive signals, and optic flow, to actively update position and heading as one travels from a known starting position, often a home or a nest [2Gallistel C.R. The Organization of Learning. The MIT Press, 1990Google Scholar, 6Mittelstaedt M.-L. Mittelstaedt H. Homing by path integration in a mammal.Naturwissenschaften. 1980; 67: 566-567Crossref Scopus (388) Google Scholar, 7Etienne A.S. Jeffery K.J. Path integration in mammals.Hippocampus. 2004; 14: 180-192Crossref PubMed Scopus (336) Google Scholar]. Landmark-based piloting, on the other hand, involves the use of allothetic (external) cues for updating [2Gallistel C.R. The Organization of Learning. The MIT Press, 1990Google Scholar]. Reorientation comes into play when one’s spatial updating — either from path integration or from landmarks — becomes inaccurate. It is then necessary to re-establish one’s coordinates de novo using allothetic cues. This can involve recovery of heading direction, location, or both. In this review, we will use the term reorientation as it is commonly used in the colloquial sense to encompass both functions. Formally, however, one should distinguish between heading retrieval and self-localization and, as we will see, between self-localization in the local sense — for example, where am I within the room? — and the global sense — for example, which room am I in? (Figure 1). Reorientation is only relevant for navigators using a cognitive-map-based wayfinding strategy. Navigators using more basic strategies, such as beaconing (moving directly to a goal) [8Leonard B. McNaughton B.L. Spatial representation in the rat: Conceptual, behavioral, and neurophysiological perspectives.in: Kesner R.P. Olton D.S. Neurobiology of Comparative Cognition. 1990: 363-422Google Scholar], view matching (moving to reduce the perceptual discrepancy between the current view and the view at the goal location) [9Collett M. Chittka L. Collett T.S. Spatial memory in insect navigation.Curr. Biol. 2013; 23: R789-R800Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar], or route following (a procedural strategy in which one implements a fixed series of actions in response to specific cues) [10Cook D. Kesner R.P. Caudate nucleus and memory for egocentric localization.Behav. Neural Biol. 1988; 49: 332-343Crossref PubMed Scopus (0) Google Scholar], do not require reorientation, as in these cases there are no internal spatial coordinates to recover. In this review, we will discuss the cognitive and neural mechanisms that underlie spatial reorientation. Our aim is to synthesize results from animal behavior, human psychology, electrophysiology, and cognitive neuroscience into a unified view of the topic. We will focus first on the behavioral literature, next on the neural correlates of reorientation within the brain’s spatial representation system, and finally on the brain systems that mediate the interaction between visual and spatial codes. We end with a brief assessment of prospects for future research. Psychologists and ethologists have learned much about the cognitive mechanisms underlying spatial reorientation by observing the behavior of humans and animals. In this section, we describe how behavioral work has illuminated three central questions about spatial reorientation: what are the external cues used for reorientation? What are the internal reference frames recovered? And is reorientation supported by a single cognitive mechanism or multiple mechanisms? Although our surroundings provide us with many cues that could in principle be used for reorientation, such as nearby objects (for example, a mailbox), distal objects (for example, a mountain), and celestial bodies (for example, the North Star), laboratory experiments suggest that reorientation behavior is often guided primarily by the spatial geometry of the environment. This fact was first discovered by Cheng and Gallistel, who observed that after misorientation [11Cheng K. A purely geometric module in the rat’s spatial representation.Cognition. 1986; 23: 149-178Crossref PubMed Scopus (737) Google Scholar] or disorientation [12Margules J. Gallistel C.R. Heading in the rat: Determination by environmental shape.Anim. Learn. Behav. 1988; 16: 404-410Crossref Google Scholar], rats in a rectangular chamber would often attempt to retrieve a buried reward by digging in the location that was diagonally opposite the correct location (Figure 2A). This behavior is notable because the correct location and the diagonally opposite location are indistinguishable if the only information the animal has to orient themselves is the geometry of the chamber as defined by the walls. The animals did not appear to use non-geometric features, such as odors, visual patterns, or wall colors, to resolve this geometric ambiguity, although they could learn an association between the reward and a feature that was co-located with it. This tendency to rely on the shape of space for reorientation has been subsequently observed in a number of species, including fish [13Sovrano V.A. Bisazza A. Vallortigara G. Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish.Cognition. 2002; 85: B51-B59Crossref PubMed Scopus (160) Google Scholar], human children [14Hermer L. Spelke E.S. A geometric process for spatial reorientation in young children.Nature. 1994; 370: 57-59Crossref PubMed Scopus (427) Google Scholar], and human adults tested under conditions that place demands on language and working memory [15Hermer-Vazquez L. Spelke E.S. Katsnelson A.S. Sources of flexibility in human cognition: Dual-task studies of space and language.Cognit. Psychol. 1999; 39: 3-36Crossref PubMed Google Scholar, 16Ratliff K.R. Newcombe N.S. Is language necessary for human spatial reorientation? Reconsidering evidence from dual task paradigms.Cognit. Psychol. 2008; 56: 142-163Crossref PubMed Scopus (57) Google Scholar]. Experiments in avian species and monkeys, on the other hand, have observed more equal reliance on geometric and non-geometric features [17Vallortigara G. Zanforlin M. Pasti G. Geometric modules in animals’ spatial representations: A test with chicks (Gallus gallus domesticus).J. Comp. Psychol. 1990; 104: 248Crossref PubMed Google Scholar, 18Gouteux S. Thinus-Blanc C. Vauclair J. Rhesus monkeys use geometric and nongeometric information during a reorientation task.J. Exp. Psychol. Gen. 2001; 130: 505Crossref PubMed Google Scholar]. On the basis of their results, Cheng and Gallistel hypothesized that reorientation is supported by a geometric module that exclusively uses the shape of surrounding space to re-establish heading after misorientation or disorientation, and is impenetrable to non-geometric featural cues. This idea has generated considerable discussion over the past 30 years, in part because of the broader theoretical significance of the modularity claim. It is now clear that non-geometric cues can have an important influence over behavior after disorientation in many species; for example, when 18–24-month-old children search for a hidden toy they exhibit the classic result of failing to use a visual feature (a single colored wall) to disambiguate between geometrically equivalent locations in a small (4 x 6 feet) rectangular room, but they will use the same feature to distinguish between the locations in a large (8 x 12 feet) room [19Learmonth A.E. Nadel L. Newcombe N.S. Children’s use of landmarks: Implications for modularity theory.Psychol. Sci. 2002; 13: 337-341Crossref PubMed Google Scholar]. It remains debated, however, whether this use of non-geometric features reflects incorporation of non-geometric information into reorientation [20Cheng K. Huttenlocher J. Newcombe N.S. 25 years of research on the use of geometry in spatial reorientation: a current theoretical perspective.Psychon. Bull. Rev. 2013; 20: 1033-1054Crossref PubMed Scopus (68) Google Scholar] or the operation of a separate post-reorientation mechanism that checks the features at the target location for consistency with visual memory [21Lee S.A. Spelke E.S. Two systems of spatial representation underlying navigation.Exp. Brain Res. 2010; 206: 179-188Crossref PubMed Scopus (51) Google Scholar]. For our purposes, it is not important to resolve this debate, but merely to note that the literature indicates that environmental geometry is a powerful cue for reorientation. There are at least three reasons why geometry may be particularly important for reorientation. First, environmental shape — the topography of the landscape — is an inherently stable aspect of the environment [2Gallistel C.R. The Organization of Learning. The MIT Press, 1990Google Scholar]. Indeed, there is evidence that the navigational system distinguishes between stable and unstable objects, using only the former as spatial references [22Biegler R. Morris R.G. Landmark stability is a prerequisite for spatial but not discrimination learning.Nature. 1993; 361: 631-633Crossref PubMed Scopus (107) Google Scholar]. Second, boundary geometry tends to cover a large field of view and hence is perceptually salient. Third, geometry may be especially useful for a disoriented navigator because the intrinsic shape of the environment can be used to define an orientational axis [23Cheng K. Gallistel C.R. Shape parameters explain data from spatial transformations: comment on Pearce et al. (2004) and Tommasi & Polli (2004).J. Exp. Psychol. Anim. Behav. Process. 2005; 31: 254-259Crossref PubMed Scopus (0) Google Scholar]. Discrete landmarks, on the other hand, only define a consistent direction if they are distal from the viewer [1O’Keefe J. Nadel L. The Hippocampus as a Cognitive Map. Clarendon Press Oxford, 1978Google Scholar] (which may explain why nongeometric features have a stronger effect in larger environments). Interestingly, discrete landmarks are useful for spatial updating in oriented animals [24Suzuki S. Augerinos G. Black A.H. Stimulus control of spatial behavior on the eight-arm maze in rats.Learn. Motiv. 1980; 11: 1-18Crossref Google Scholar], even if they are less useful for reorientation, because the bearing between the observer and the landmark defines a unique direction in space if the locations of both the observer and the landmark are known [25Bicanski A. Burgess N. Environmental anchoring of head direction in a computational model of retrosplenial cortex.J. Neurosci. 2016; 36: 11601-11618Crossref PubMed Google Scholar]. Moreover, it is possible that discrete landmarks might be more important for reorientation in natural environments, which tend to be more open than the restricted enclosures that are almost universally used in laboratory experiments [26Lew A.R. Looking beyond the boundaries: time to put landmarks back on the cognitive map?.Psychol. Bull. 2011; 137: 484Crossref PubMed Scopus (43) Google Scholar]. Location and heading — the quantities recovered during reorientation — must be defined relative to a reference frame. Some insight into these reference frames has come from studies using the judgment-of-relative-direction task [27Kozlowski L.T. Bryant K.J. Sense of direction, spatial orientation, and cognitive maps.J. Exp. Psychol. Hum. Percept. Perform. 1977; 3: 590Crossref Scopus (0) Google Scholar]. Subjects in these experiments first learn an environment containing several objects. They are then removed from the environment and asked to imagine that they are standing at one object while facing a second; they then point to a third object. To perform this task, subjects must mentally re-instantiate a location and heading on each trial — a task akin to reorientation. Because they do this in the absence of relevant perceptual cues — trials are performed outside the recalled environment — the task illuminates the internal representations used during reorientation. A consistent result from these experiments is that performance is orientation-dependent; that is, accuracy varies as a function of imagined facing direction. In some experiments, one imagined direction is preferred, while in others, directions opposite or orthogonal to this direction are also preferred, but to a lesser extent [28McNamara, T.P. (2002). How are the locations of objects in the environment represented in memory? In International Conference on Spatial Cognition (Springer), pp. 174–191.Google Scholar]. For example, in one study examining judgment-of-relative-directions defined by buildings on a college campus with a north–south alignment, accuracy was greatest for north-facing views, and it was also greater for east, south, and west facing views than for views facing diagonal directions [29Marchette S.A. Yerramsetti A. Burns T.J. Shelton A.L. Spatial memory in the real world: long-term representations of everyday environments.Mem. Cognit. 2011; 39: 1401Crossref PubMed Scopus (19) Google Scholar] (Figure 2B). The advantage for the preferred directions is observed across different imagined standing positions, thus indicating that the preference is for a direction rather than for a specific view. These results have been interpreted as evidence that we assign spatial axes to environments when we first encounter them, which we then use to orient ourselves when we encounter them again, or (in this case) imagine encountering them. Spatial recall is more accurate for imagined views that are aligned with these axes than for imagined views that are misaligned. Notably, environmental geometry plays an important role in defining these axes, though other factors are also influential, including egocentric experience (the direction that one first enters an environment is often privileged, especially if it is aligned with local geometry) [30Shelton A.L. McNamara T.P. Systems of spatial reference in human memory.Cognit. Psychol. 2001; 43: 274-310Crossref PubMed Scopus (0) Google Scholar], the arrangement of objects within a room [31Mou W. McNamara T.P. Intrinsic frames of reference in spatial memory.J. Exp. Psychol. Learn. Mem. Cogn. 2002; 28: 162Crossref PubMed Google Scholar], and even the intrinsic alignment of these objects [32Marchette S.A. Shelton A.L. Object properties and frame of reference in spatial memory representations.Spat. Cogn. Comput. 2010; 10: 1-27Crossref Scopus (17) Google Scholar]. These results suggest that — in humans at least — these axes are established by a cognitive mechanism that is sensitive to several different kinds of spatial organization in the visually perceived environment, including the shape of local space, but also other factors. We have been discussing reorientation as a single process; there is, however, some evidence that it might be divisible into separate subcomponents. Heading retrieval and self-localization are logically dissociable from each other: a compass indicates heading but not location, whereas a global positioning system indicates location but not heading. Under some circumstances, animals use different cues to solve each problem. In the Morris Water Maze, for example, when rodents are placed into a circular pool at random locations and must navigate to a hidden platform, they use distal cues provided by the surrounding experimental room (including, potentially, its shape) to determine their heading, while using proximal cues provided by distance to the wall of the pool to determine their location [33Hamilton D.A. Akers K.G. Weisend M.P. Sutherland R.J. How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector.J. Exp. Psychol. Anim. Behav. Process. 2007; 33: 100Crossref PubMed Scopus (0) Google Scholar, 34Knierim J.J. Hamilton D.A. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation.Physiol. Rev. 2011; 91: 1245-1279Crossref PubMed Scopus (61) Google Scholar]. That is, they use the cues that are most informative to solve each component of the task. Additional evidence for multiple reorientation mechanisms comes from a recent study from our lab, which focused on the distinction between heading retrieval and context recognition [35Julian J.B. Keinath A.T. Muzzio I.A. Epstein R.A. Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice.Proc. Natl. Acad. Sci. USA. 2015; 112: 6503-6508Crossref PubMed Scopus (15) Google Scholar]. The idea here is that reorientation involves not only determining one’s heading and location on a cognitive map, but also recognizing which cognitive map to retrieve. To demonstrate a dissociation between these two functions, we trained mice on a novel version of the Cheng and Gallistel reorientation task in which there were two rectangular chambers, rather than one, each with a different reward location. Each chamber had a distinct visual pattern along one of the walls, which was potentially informative about both heading (because the location of the pattern broke the geometric symmetry of the chamber) and contextual identity (because the patterns in each chamber were different). Strikingly, the search behavior of the animals indicated that they used the visual pattern to distinguish between the chambers, but did not use the pattern to distinguish between geometrically equivalent headings within each chamber (Figure 2C). This demonstrates a dissociation between heading retrieval and context recognition, insofar as these functions are controlled by different cues. As conceptualized above, reorientation involves recovery of location on a cognitive map and facing direction relative to the map’s coordinate system. To understand the neural basis of this phenomenon, we must consider how reorientation affects the neural systems that mediate the cognitive map. Over forty years of neurophysiological research have identified neurons in the rodent brain that are believed to be crucial for cognitive-map based navigation [36Grieves R.M. Jeffery K.J. The representation of space in the brain. Behav.Processes. 2017; 135: 113-131Crossref PubMed Scopus (0) Google Scholar, 37Hartley T. Lever C. Burgess N. O’Keefe J. Space in the brain: how the hippocampal formation supports spatial cognition.Philos. Trans. R Soc. B. 2014; 369: 20120510Crossref PubMed Scopus (0) Google Scholar], with recent evidence suggesting a similar organization in humans [38Epstein R.A. Patai E.Z. Julian J.B. Spiers H.J. The cognitive map in humans: spatial navigation and beyond. Nat.Neurosci. 2017; 20: 1504PubMed Google Scholar]. These neurons include: place cells in the hippocampus, which fire when the animal is in specific locations within the environment [39Ekstrom A.D. Kahana M.J. Caplan J.B. Fields T.A. Isham E.A. Newman E.L. Fried I. 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Representation of geometric borders in the entorhinal cortex.Science. 2008; 322: 1865-1868Crossref PubMed Scopus (471) Google Scholar, 46Lever C. Burton S. Jeewajee A. O’Keefe J. Burgess N. Boundary vector cells in the subiculum of the hippocampal formation.J. Neurosci. 2009; 29: 9771-9777Crossref PubMed Scopus (273) Google Scholar]. Although the full range of functionality of these systems remains a topic of considerable debate, with much recent evidence suggesting that they do more than simply represent physical space [47Aronov D. Nevers R. Tank D.W. Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit.Nature. 2017; 543: 719-722Crossref PubMed Scopus (62) Google Scholar, 48Constantinescu A.O. O’Reilly J.X. Behrens T.E. Organizing conceptual knowledge in humans with a gridlike code.Science. 2016; 352: 1464-1468Crossref PubMed Scopus (168) Google Scholar, 49Nau M. Schröder T.N. Bellmund J.L. Doeller C.F. Hexadirectional coding of visual space in human entorhinal cortex.Nat. Neurosci. 2018; : 1PubMed Google Scholar, 50Julian J.B. Keinath A.T. Frazzetta G. Epstein R.A. Human entorhinal cortex represents visual space using a boundary-anchored grid.Nat. Neurosci. 2018; 21: 191-194Crossref PubMed Scopus (2) Google Scholar], it is generally accepted that in the navigational realm, place cells allow different locations and environments to be distinguished from each other, grid cells allow distances between locations to be defined, head-direction cells allow the animal to represent a heading relative to a consistent reference frame, and border/boundary cells allow spatial codes to be referenced to fixed topographical elements such as chamber walls. Within a given environment, hippocampal place cells exhibit unique preferred firing locations, known as ‘place fields’, with reliable relationships between the preferred locations of different cells. Thus, one can speak of the orientation and translational position of this hippocampal map relative to the external environment. Reorientation then corresponds to the recovery of a previously held map orientation and translational position following disorientation. What are the external cues that are relevant to the recovery of map orientation? Many studies have shown that objects at the extremities of the perceptible environment are strong controllers of the orientation of the hippocampal map. Place fields rotate their locations around the center of the experimental chamber when objects in the surrounding room or along the walls of the chamber are rotated between navigational episodes [34Knierim J.J. Hamilton D.A. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation.Physiol. Rev. 2011; 91: 1245-1279Crossref PubMed Scopus (61) Google Scholar, 51O’Keefe J. Conway D.H. Hippocampal place units in the freely moving rat: why they fire where they fire.Exp. Brain Res. 1978; 31: 573-590Crossref PubMed Google Scholar, 52Cressant A. Muller R.U. Poucet B. Failure of centrally placed objects to control the firing fields of hippocampal place cells.J. Neurosci. 1997; 17: 2531-2542Crossref PubMed Google Scholar]. Moreover, when distal cues, chamber geometry, and the internal sense of direction of the animal are rotated relative to each other, thus placing them into conflict, place cells exhibit mixed behavior, sometimes rotating with the chamber, sometimes with the distal cues, and sometimes remapping entirely [53Jeffery K.J. Donnett J.G. Burgess N. O’Keefe J.M. Directional control of hippocampal place fields.Exp. Brain Res. 1997; 117: 131-142Crossref PubMed Scopus (69) Google Scholar]. At first glance, these findings would seem to be at odds with the behavioral data, suggesting that reorientation behavior is primarily controlled by environmental geometry. However, an important feature of most of these recording experiments is the fact that the animals are typically not disoriented before being placed back in the chamber. Thus, most studies of the effect of environmental cues are studies of orien" @default.
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• W2890141662 date "2018-09-01" @default.
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• W2890141662 title "The Neurocognitive Basis of Spatial Reorientation" @default.
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