Psychology of spatial cognition.

Overview

Psychology of spatial cognition Luca Tommasi1∗ and Bruno Laeng2 In this overview, focusing on memory and higher cognitive processes, we cover some of the most relevant results that emerged from research on spatial cognition in animals and in humans in the last 3 decades. In particular, we discuss how representations of distance and direction are used to localize oneself with respect to the external world, to determine the position of objects with respect to each other, and to compute the position of invisible goals. The role of landmarks and environmental geometry as cues for extracting spatial information in such abilities is compared, and the reliance upon self-centered and external frames of reference is discussed. Moreover, the contribution of working memory and processing strategies in forming representations of spatial relations in humans is presented. Finally, implications for some neighboring fields of the cognitive sciences will be outlined. © 2012 John Wiley & Sons, Ltd. How to cite this article:

WIREs Cogn Sci 2012, 3:565–580. doi: 10.1002/wcs.1198

INTRODUCTION

I

f we open a handbook of philosophy and search for conceptualizations of space proposed in the history of thought, we find out that philosophers debated to a great extent about the very idea of space, as if it were a category somewhat in need of extra effort. Importantly, accompanying this debate since its inception, references to axiomatic definitions of space, most noticeably emerging from mathematics and physics, were often contrasted to a personal, intuitive understanding of space. Actually, the subjective dimension of space (the same might be said for time) has constituted a sort of unwanted perturbation in the process of reaching toward an objective definition that could be satisfactory for those interested in understanding the universe rather than the laws of experience. However, the idea that space is at the same time objective and subjective has a long history of disputes, whose resolution for the cognitive sciences was pioneered by Hermann von Helmholtz and Ernst Mach, in the period that saw the birth of experimental psychology. Both von Helmholtz1 and Mach2,3 reconciled the two faces of the coin, proposing that both subjective (intuitive) and objective ∗ Correspondence

to: [email protected]

1

Department of Neuroscience and Imaging, University of Chieti, Chieti, Italy 2

Department of Psychology, University of Oslo, Oslo, Norway

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(physical) space can and should be understood by means of empirical investigation, thus paving the way to a fruitful dialogue between ‘abstract’ geometry and the study of ‘concrete’ space as experienced by perception and cognition.4 From then on, space became a key topic of psychological inquiry first and a major theme of cognitive science later. As a field of investigation in its own right, spatial cognition has witnessed a tremendous increase in interest since the 1970s, merging research about many levels of mental function (from perception to memory and higher cognitive phenomena), in both animals and humans. Broadly defined, it could be identified as the study of mental representations and processes evolved in living organisms to cope with the physical dimension of space, be it the space immediately experienced through a sensory modality (visual space, auditory space, etc.) or the whole environment in which behavior has its course. But what are the issues faced by the study of spatial cognition? Such a question seems to point to answers that are very down-to-earth, as they are linked tightly to the unavoidable association between the existence of living organisms and the fact that their behavior takes place in space. However trivial this may appear, space is occupied by objects and other organisms, and it is necessary to take into account their position in order to perform behaviors, plan movements, or simply evaluate events happening in the environment. Thus, a first aspect that should be

© 2012 John Wiley & Sons, Ltd.

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Overview

understood is how organisms compute where things are with respect to themselves, and vice versa. A second aspect could be described as computing where things are with respect to each other. It must be remarked that space is a dimension cutting across multiple psychological constructs, from perception to higher cognitive processes. Appreciating positions of things with respect to oneself is something crucial in perception, attention, and motor planning, when space is experienced directly and must be computed as an external source of information. But space is computed also, and perhaps to a larger extent, in the absence of sensory information, such as in those cases in which the task is reaching an invisible goal or in which spatial imagery is used to appreciate places that do not exist in reality, such as while reading the description of the settings of Alice in Wonderland. As these aspects are relevant for all living organisms, it is not surprising that a common ground of studies on spatial cognition and its consequences on behavior grew steadily both in biology and in psychology since the second half of the 19th century. Experiments on animals were important for elucidating the basic mechanisms of spatial learning and cognition (typically in the psychologist’s laboratory), whereas animal observation and field studies could reveal how those mechanisms are exploited during orientation and navigation in the wild (topics more familiar to biologists). Moreover, many laboratory paradigms turned out to be important tools for the neurosciences, as the interest increasingly focused on the neural bases of spatial cognition during the last decades of the 20th century. The first section of this overview will present some aspects of spatial cognition that were the result of studies on animals—from insects to primates—illustrating which spatial information is represented and exploited in simple laboratory settings. Studies on humans have paralleled the interest for the basic mechanisms of spatial cognition in other animals, but have also focused more specifically on issues of spatial processing relevant for the understanding of human cognitive architecture. In cognitive psychology, many models of human spatial representation and cognition have been proposed, often integral to more comprehensive models of human attention, memory, imagery, and higher cognitive phenomena. The second section of this overview will deal with some selected aspects of spatial cognition that received particular attention in humans, from the notion of frame of reference and its dependence upon self-centered and external information, passing by the role of working memory 566

and strategies in forming representations of space, to the difference between coordinate and categorical spatial relations. Beyond the study of spatial cognition as a set of mechanisms and processes underlying the animal and human cognitive worlds, numerous interface domains have become of great interest because they feed from results in animal and human studies, increasing the knowledge stemming from psychological research in a virtuous circle that rewards the breaking of disciplinary boundaries. One obvious interface area concerns the study of the neural bases of spatial cognition, as the fast progress in neuroscience continues to elucidate the mechanisms that subserve spatial functions at the level of cells, circuits, and brain networks. A second area involves the interaction between the psychology of spatial cognition and robot design, an interplay that aims at creating machines capable of navigating in the environment through the recourse of perception, storing and retrieval of information, and planning. These topics will be briefly reviewed in the final section.

ANIMAL MODELS OF SPATIAL COGNITION Animal orientation and navigation, including longdistance migration and homing in a variety of species, have attracted the interest of scientists and naturalists for centuries.5,6 A key aspect of these phenomena is the fact that sensory information beyond the grasp of human perceptual experience seems to be exploited with a high degree of precision by navigating organisms traveling for even thousands of miles. Basic types of orienting behaviors involve reactive movements directed toward or away from an energy source, such as in tropisms, taxes, and kineses.7 Animal spatial orientation relies upon stable frames of reference gathered by some sensory input and compensated from time to time, in order to correct for possible accumulating errors, by switching to other modalities. Despite the use of magnetic, mechanical, thermal, and other sensory systems for long-range navigation, vision is one of the most widespread primary sources of information for navigation over shorter spatial ranges in the majority of vertebrates, but also in invertebrates. Moreover, when an animal uses its currently perceived position in order to compare it to an internal image of the external world (mnemotaxis), it is clear that some form of spatial representation is being used. Thus, perception, learning, and memory are all important aspects that can be put into play in experiments to reveal how these representations are shaped.



WIREs Cognitive Science

Psychology of spatial cognition

Laboratory and field studies in animals have traditionally exploited two methods for studying the spatial cognition of animals: mazes and open fields. In a maze, in which alleys and multiple choice points force the animal to follow precise paths and to make choices at precise locations, a goal can be reached by the adoption of a series of correct decisions at given choice points. An open field is usually an environment (arena, enclosed space, etc.) that can be endowed with a number of objects inside and/or outside its boundaries and that can be freely explored. The localization of a place in an open field, differently than in a maze, typically takes place with reference to distances and directions to other internal and external objects. O’Keefe and Nadel8 proposed two strategies adopted to reach a goal and optimally suited to the two types of environments: the taxon system (the encoding of the series of successive responses that allow to reach for the goal along a route, as in the maze) and the locale system (the mapping of spatial relationships between positions that could pinpoint to the goal, as in an open field).

Landmarks In a maze, but more likely in an open field, spatial representations depend heavily on the visual perception, the encoding, and the retrieval from memory, of landmarks.9 Landmarks can be objects or salient aspects of the environment that are used as spatial references to recover the position of otherwise featureless places. A landmark offers a visual affordance to distance mapping in the environment as long as it is perceptible and does not move. Moreover, distance from a familiar landmark is perceived directly as a parameter of retinal size, and we know that distance estimation is among the few psychophysical dimensions that are neither compressive nor expansive, but linear (the subjective counterpart is neither underestimated nor overestimated when the objective magnitude changes)—it is a reliable measurement of objective distance.10–12 The distance of the animal from a landmark is thus a first relevant factor in spatial cognition. If a goal is spatially contiguous to the landmark, navigating to that goal simply means approaching the landmark. More often, however, goals are located at some distance and direction from one or more landmarks, and they are invisible to the animal because they are too far away or because they are hidden or concealed by something else. In this case, the position of the goal has to be deduced by computing the distance and the direction of the goal from the animal, with reference to the Volume 3, November/December 2012

visible landmark/s. Provided that searching behavior successfully concentrates at the goal location as a consequence of learning with respect to a given spatial arrangement of landmarks, the possibility of transforming the original position or appearance of the landmarks and checking for changes in the spatial distribution of searching behavior allow the experimenter to deduce the contribution of landmark information in representing spatial positions. In some seminal experiments carried out by Tinbergen,13 for instance, digger wasps of the species Philantus triangulum were accustomed to the presence of pine cones arranged in a circle around the nest during their peregrinations in and out of it. Wasps of this species are ‘central-place foragers’, which means that they depart and return to a stable position in space (the nest) for provisioning food for their larvae that are safely hidden in the nest. When Tinbergen shifted away the pine cones during the wasps’ outward journeys, returning wasps searched for the burrow of the nest at the center of the novel location of the circle, demonstrating that they relied upon the presence of the pine cones as visual landmarks pinpointing to their goal (Figure 1). In tests on single landmark-based orientation, honeybees (Apis mellifera) trained to find a sucrose reward at a given distance and direction from a cylinder, searched randomly when the cylinder was removed, but searched at proportional distances when the cylinder was replaced with a larger or a smaller replica14 (Figure 2(a)) Similar experiments carried out on Mongolian gerbils (Meriones unguiculatus) showed that only in tests carried out after a reduction in size of the landmark, the gerbils scaled their search behavior (searching at a shorter distance from it), but this did not happen when the landmark was replaced with an enlarged replica, in which case they searched at the same distance from it as with the original landmark15 (Figure 2(b)). These experiments showed that distance and direction from a single landmark are spatial information that can be gathered and used for localization in invertebrates as well as in vertebrates, although they lend support to the existence of different orienting mechanisms between insects and other species. According to the results obtained in bees and in many species of ants,16 it was proposed that a mechanism based on the reduction of discrepancy between the current view and stored views of the goal from a number of vantage points would suffice to accomplish visual orientation toward the goal.17 Despite the fact that a view could include a number of discrete parts, it is likely that ants use a broad panoramic representation of some


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Nest

FIGURE 1 | Tinbergen’s experiment on

homing in digger wasps.13 Above: a digger wasp (Philantus triangulum) homing to its nest, surrounded by a circle of pine cones. Below: when the pine cones are shifted to a different location, the wasp directs its flight to the middle of the circle, showing that the position of the nest was encoded relative to the pattern of pine cones.

Nest

kind in route navigation, likely without parsing any objects or landmarks in it.18 The result of incomplete distance scaling shown in gerbils with landmark size transformations proved that the mere retinotopical information provided by the visual scene was not the only cue used by the gerbils to orient to the goal. Similar results were obtained with pigeons (Columba livia),19,20 thus suggesting that landmark orientation in higher vertebrates, differently than in insects, cannot depend uniquely on a mechanism based on distance estimation that is in turn based on retinal size. Collett et al.15 proposed a model (the vector sum model), according to which the position of a goal would be encoded as the sum of all vectors (including distance and direction) from all nearby landmarks. The plausibility of the vector sum model has been tested (and most often confirmed) in birds,20,21 and its most recent version based on experiments in pigeons captures the reliance of this species both upon ‘true’ vectors, that is distances and directions to a goal from discontinuities in the environment (corners, edges, and landmarks), and also upon perpendicular distances between walls and landmarks20 (see Figure 3). Experiments with dogs (Canis familiaris) tried to precisely quantify the contribution of walls and landmarks in determining distance and direction to a hidden goal located equidistantly between the two cues. By exploiting transformation tests that involved the perpendicular or diagonal shifting of the landmark, it was shown that the dogs distributed their searching behavior by averaging the distance from the walls and the landmark,22 showing that the encoding of distance and direction from surfaces might be as relevant as 568

that from landmarks, as it will be shown in the next section. Many studies made use of pairs of landmarks with respect to which a hidden goal had to be found (i.e., in the middle between the landmarks, in a noncentral position along the symmetry axis dividing them, and in positions defining the apex of an irregular triangle) and also of larger arrays of landmarks. Pigeons, for example, were successful at localizing a goal positioned along the symmetry axis of two landmarks as if it were on the apex of an isosceles triangle, but when the distance between landmarks was changed during test trials, they failed to scale their spatial search to the novel distance between the landmarks, searching at the learned distance and direction from either landmark.23 This result seems to confirm the evidence of a number of studies in many species that investigated the reliance on individual landmarks or subsets of them, after successful training with a landmark array: spatial search may turn out to be based either on the entire configuration or on individual landmarks or on parts of the array.15,24–27 Importantly, results of experiments carried out in invertebrates indicate that snapshot-matching mechanisms depending on the retinal projection of the landmarks might account for the ability to orient also with reference to a landmark array, because the search patterns observed after expansion tests crucially depend upon the fact that landmark size is left unaltered or it is accordingly expanded during the tests28–30 (Figure 4). If, on the one hand, the sensory mechanisms of landmark-based orientation are still debated, on the functional side the utilization of arrays of landmarks





(a) v1

p2

h

G

p1

v2

h /2

FIGURE 3 | An example of the vector sum model, as derived from

2h

(b)

data on pigeons. The two rectangles represent two wooden blocks located by the wall in an enclosure (larger frame). The position of the goal G is determined by vector summation of the two vectors v1 and v2 , respectively, encoding distance and direction from a corner and an edge. The goal G is also defined by the intersection of the two lines, p1 and p2 , perpendicular to the nearby surfaces (albeit with different weights according to distance, as reflected by the thickness of the lines). (Reprinted with permission from Ref 20. Copyright 2006 Elsevier)

h

h /2

2h

FIGURE 2 | Reaction of bees (Apis mellifera) and gerbils (Meriones

unguiculatus ) to contraction and expansion in size of a landmark.14,15 (a) After learning the position of a sucrose dish located close to a landmark (above), halving the size (middle) or doubling the size (below) of the landmark results in proportional shifts of the searching behavior of bees. (b) With a similar paradigm, gerbils trained to uncover a sunflower seed, proportionally adapt their searching behavior after the reduction but not after the expansion in size of the landmark.

has obvious advantages. For many food-storing avian species, such as the Clark’s nutcracker (Nucifraga columbiana), encoding positions with reference to multiple landmarks is particularly important for retrieving the countless food caches previously hidden in the ground.31 In fact, when a goal is defined with respect to more than one available landmark, the higher number of spatial references increases the precision with which both distance and direction to the goal can be estimated.32 Reliance upon two landmarks was observed in Clark’s nutcrackers trained to find a goal at different points between the landmarks or trained to find the apex of a triangle on the basis of either direction or distance.33 The interlandmark distance was varied across training trials (choosing Volume 3, November/December 2012

from a set of values) and animals learned to solve the task properly. When novel interlandmark distances were used during test trials, they showed accurate search also with the novel distances. When tested with new orientations of the landmarks, the birds tended to follow small but not large rotations. Finally, when tested with a single landmark, birds that had been trained to use a constant bearing searched in the appropriate direction from the landmark, but birds that had been trained to use distance failed. The logics of this type of experiment, in which training interlandmark distances were chosen from a given set, and distances at test were novel, might not capture entirely the operations of landmark-based orientation that usually take place in the wild, but have certainly offered a reliable evaluation of the degree of reliance upon objects that occur during visual orientation in these species, in particular as regards the use of absolute spatial information (i.e., learning and using ‘inflexibly’ the distance and/or direction from one landmark) and the use of relational spatial information, such as in the case of following some sort of proportionality rule (i.e., that the goal is ‘halfway’ between two landmarks). Reliance upon multiple landmarks is particularly important for determining direction, because it has been demonstrated that the precision of directional information, as it should be expected, is strongly influenced by the distance of the goal from a landmark:34 the farther the goal from it, the larger the probability that the search will be aimed in the wrong direction. Although distance errors (assuming a correct heading) can be easily fixed (by a rule such as ‘walk back and forth along the established direction’), it may be not as easy to fix heading errors (assuming


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Overview

Training

Test with double distance and unmodified landmarks

Test with double distance and double landmarks

FIGURE 4 | Reactions of ants of the species Melophorus bagoti to contraction and expansion of a landmark array and landmark size. After training to find a goal in the middle of a four-landmark array (left), the landmark array is expanded (the distances are doubled) leaving the size of landmarks unaltered (middle) or also doubling the size of landmarks (right). Searching behavior is represented as more or less spatially concentrated by the size and density of texture of gray areas. Examples of individual trajectories are also represented. (Reprinted with permission from Ref 30. Copyright 2007 Springer Verlag)

a correct distance), which would presume a rule such as ‘walking in a circle centered on the goal, keeping the distance fixed’.

Environmental Geometry In the studies described above, it was evident that a methodological caveat consisted in ensuring that place learning was controlled exclusively by the landmarks in the training/testing environment, trying to exclude as much as possible the influence of further objects or the surrounding environment itself. However, when the sources of information deriving from the landmarks and the environment are not kept separate by the efforts of the experimenter, spatial orientation can be largely driven also by the global shape of the environment, as shown in the experiments on landmarks and walls carried out in birds and dogs. The space inside which training takes place in many experiments is usually made of surfaces that have a spatial shape of their own. Walls, corners, and edges offer a global framework for spatial orientation extending beyond the space of local landmarks. In domestic chicks (Gallus gallus), for instance, even when a single landmark had the role of a beacon (in the center of a square-shaped enclosure), thus indicating exactly where some hidden food could be found by ground scratching on the sawdust substrate, the removal of the beacon at test trials was followed by searching behavior at the position where it had been found before, and this had to be necessarily based upon the encoding of the spatial position with reference to the surfaces of the enclosure during training35 (see also Ref 36 for similar results with 570

multiple landmarks). This ‘latent’ learning based on the arrangement of the surrounding surfaces was shown to be not so latent, given that in another experiment the global frame of reference, rather than the beacon itself, proved to be more in control of the chicks’ searching behavior. This was apparent in test trials in which the central beacon used during training was shifted to a novel position in the enclosure during test trials: chicks kept searching in the center of the enclosure, ignoring the beacon shifted toward one of the corners27 (see also Ref 37 for similar results with multiple landmarks). The possibility that landmarks and extended surfaces might entail two different encoding systems in animal spatial representation is at the core of current research, but in a recent review summarizing the literature on landmark- and surface-based spatial cognition, Lew38 proposed that landmarks and surfaces can be treated similarly in explaining spatial orientation, without the need of invoking separate learning mechanisms for either type of information. Orientation based on the geometry of surfaces has become one of the most fruitful topics of spatial cognition, since the initial intuition that led Cheng to pioneer a paradigm based on a rectangular enclosure, originally tested in rats (Rattus norvegicus), and bringing the hypothesis of the geometric module.39 The terms ‘rectangular’ and ‘enclosure’ both convey crucial aspects behind the idea (see Figure 5). First, the environment chosen by Cheng was an empty enclosure, an arena built as a space surrounded by walls. This setup implied that any position that the experimenter wanted to be localized by the rat would have to be searched exclusively relying on the distance and





A

B

D

C

FIGURE 5 | Schematization of the rectangular enclosure as seen from above. Corners A and C are geometrically equivalent, as both are defined by a left wall on the left and a long wall on the right. The position of a goal (the filled circle) is systematically confused with its rotational equivalent (dashed circle).

direction information conveyed by the spatial arrangement of the walls. This constraint was subsequently satisfied by researchers replicating the experiment in a variety of species and introducing one or more differences to test specific hypotheses, but it was always ensured both that the substrate in the enclosure were homogeneous (i.e., sand, sawdust, or even water) and that extra-enclosure information were inaccessible. The second term, rectangular, catches the other pillar on which the paradigm rests: if place learning must take place in a rectangle-shaped environment, the position of a goal can be confused systematically with its rotational equivalent (i.e., a second position that bears the same relationships with respect to a long and a short wall; corners A and C in Figure 5). In both working memory and reference memory experiments, Cheng indeed demonstrated that rats confused the position of the goal and its rotational equivalent. This proves that rats had encoded metric information (long and short length of walls), and they had appropriately linked that information to sense (left and right). The crucial finding, however, consisted in observing that, in the working memory experiment, the rats confused the two geometrically equivalent positions even when the walls of the enclosure were not equally homogeneous, for instance when a wall was painted differently than other walls or when distinctive panels (different in color, texture, and even smell) were attached to the corners. In these cases, the nongeometric information provided by the lack of wall homogeneity or by the presence of the panels would have been sufficient to discriminate the goal from its rotational equivalent. Many tests involving transformations of the spatial position of panels at corners were carried out, showing that rats exploited primarily the shape of the enclosure in order to localize the goal. The finding was interpreted by Cheng as evidence of a geometric module that would blindly follow the geometric Volume 3, November/December 2012

information provided by the arrangement of walls and that would be impenetrable to other, nongeometric, information.40 One aspect of the paradigm that turned out to be very important is the fact that while the rat is moved in and out of the enclosure from trial to trial, it might benefit from the recording of vestibular information (by means of passive path integration) for localizing the goal. This should be avoided by disorienting the animal and/or by rotating the enclosure in between trials.41 The animal would thus need to reorient itself, establishing its heading with respect to the available features, before searching for the goal. This disorientation/reorientation procedure is so central to the paradigm that the majority of recent studies focus explicitly on ‘spatial reorientation’ in referring to the task. The primacy of geometric over nongeometric information and the idea of a dedicated geometric module, after the initial observations by Cheng, were repeatedly put to test by means of experiments carried out in a variety of species.9,42 Experiments with mammals other than rats (including humans),43–45 birds,46–48 fish,49,50 and even invertebrates51 have demonstrated that species differ largely in terms of their ability to encode nongeometric information, but have almost invariably shown that animals encode and use geometric information in order to reorient themselves in a rectangular enclosure. Important species differences seem to concern the ability of conjoining geometric and nongeometric information, calling into question the role of language in humans, and in particular the emergence of words denoting spatial concepts such as ‘left’ and ‘right’ (that might play a major role in exploiting remembered descriptions such as ‘the short wall to the left of the blue panel’). It was in fact observed that the reorientation task can take advantage of nongeometric information in adults, but not in preverbal infants,44 although the results in this direction have not always been consistent.45,52 One aspect that has proven crucial in modulating the encoding of nongeometric information in enclosed spaces, which was first observed in infants, is the size of the enclosure itself: when reorientation takes place in a small room, rotational errors are observed, the animal disregarding the presence of nongeometric information, but this is not the case in a larger room.45,53 Similar experiments in animals confirmed the result,54,55 suggesting that size differences might be attributed to better encoding of landmark information at a distance in larger enclosures. At the same time these studies allowed to disentangle the role of metric (i.e., long vs short wall) and sense properties (i.e., left vs right), which would be differently accessible, visual angle being


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equal, in the different sized enclosures.56 If length of surfaces plays a role in the formation of geometric representations, another metric property that is taken into account is the amplitude of angles formed by surfaces, as in the corners of the enclosures typically used in reorientation studies. Experiments carried out in nonquadrangular enclosures (i.e., parallelogramshaped) have demonstrated that domestic chicks can indeed reorient based on the amplitude of angles (acute or obtuse) formed by surfaces,57 and that this metric feature might be more relevant than surface length.58 Finally, it must be said that the idea that the geometric module fulfills the criteria of modularity40 (encapsulation, automaticity, innateness, and neural specialization) received conflicting support.9,42,59 This caused an intense debate over the issue, challenging the very notion of modularity and the possibility that geometry could truly be a core domain of mental representation, with evidence against the geometric module hypothesis accumulating at a faster rate than positive evidence.60–62

HUMAN SPATIAL COGNITION The previous section made it clear that also in humans spatial cognition is crucial for the process of reorientation involved in navigation, no less than in any other species. In this section, a broader scope will be adopted for providing the reader with a general overview on the manifold aspects of spatial cognition that have been investigated in depth in humans. Like other species, humans use spatial information for many functions, such as navigating in their environment. However, humans do not solely ‘act’ in space but, to a large extent, also engage in ‘cognizing’ about space. For example, we can think about an object being present in a place although neither the object nor the place is any longer visible (i.e., Piagetian object permanence). Similarly, differences in vantage point have to be taken into account when deciding whether another individual can see an object in an environment. This raises the importance of frames of reference for understanding spatial cognition, a topic that has been studied extensively in humans. This concept somewhat connects aspects of spatial perception and attention to processes that have revealed important aspects of how humans mentally represent and exploit space: because spatial information is gathered mainly in the visual modality, we will focus on visuospatial working memory and visuospatial imagery, also for the role they play in problem solving and in the planning of behavior. One spatial aspect that received a considerable amount of 572

attention in humans, also due to its relation to language, is the difference between the processing of coordinate and categorical relations.

Frames of Reference Frames of reference can be conceived as systems of spatial coordinates that allow an individual to establish her/his orientation with respect to the surrounding environment. For instance, all organisms are constantly subjected to gravity, and so are objects in the environment, thus the gravitational dimension imposes an axis of spatial orientation to which the human visual system is extremely sensitive.63 If gravity determines the attribution of a top and a bottom side to visual space, what can be said about the distribution of objects around the observer? Which are the axes that define their spatial relationships? Obviously, cardinal directions are conventional references that require reliance upon physical energy that humans cannot sense (geomagnetism and polarized light). The absence of physical axes across the horizontal plane that are as strongly constraining as gravity is in the vertical dimension does not prevent an observer from establishing a frame of reference based on the view of the surroundings. This egocentric frame of reference is fed by the perception of the visual scene, replenished with objects and surfaces, as seen from the momentary perspective of the observer. Similar to the use of landmarks in animals, there is substantial evidence that humans assign to parts of the environment a role as reference points,64 and that these can in turn be exploited to pinpoint spatial locations according to the immediate needs (i.e., recovering the position of an object or establishing the goal of one’s own navigation). An egocentric frame of reference depending on the current viewpoint of the observer is by definition ephemeral, as movements of the observer have the effect of altering the set of spatial relationships that originally contributed to establish it. However, if allocentric (i.e., nonegocentric) frames of references would underlie human spatial cognition, as originally implied by the very notion of a ‘cognitive map’,8,65 orientation in space would function largely as a process of adjusting one’s own position according to the reading of a reliable memory, irrespective of the temporary heading of the subject. A prior role of allocentric encoding, moreover, seems to be implausible given the fact that when subjects face the task of studying an environment filled with objects from a series of points of view, the first point of view experienced in the series assumes a special role in establishing the reference frame for subsequent





spatial decisions, most optimally when the scene contains objects aligned along a common direction or horizontal surfaces that have an intrinsic metric or that are aligned to the main axes of the environment.66 The possibility to extract spatial information from egocentric frames of reference is at the base of efficient self-localization, as it provides the observer with a precise update of visual heading during displacements, to be coupled with nonvisual cues such as those gathered by the vestibular and the proprioceptive modalities through path integration.67–69 Recollecting spatial locations with respect to one’s own position is another important consequence of possessing an egocentric frame of reference, as it allows one to compute distances and directions from the body to objects.70 Moreover, it has been ascertained that the encoding of an egocentric frame of reference, as it largely depends on vision, favors the recovery of locations that are placed in front of the observer with respect to those placed at her/his back.71 This strong reliance upon a view-based spatial frame does not prevent from creating and operating on external, orientation-independent frames of reference. However, these are more the exception than the rule: as soon as visual information permits recognition of the spatial arrangement as originally encoded in a learned view, self-centered representations prevail.72 Moreover, it was found that providing a layout of objects with an intrinsic spatial structure (thus creating a salient perceptual configuration) is not a factor favoring the reliance upon an external frame of reference.73 However, data from neuroimaging confirm the coexistence of two processing systems that support the use of both types of frames in the human brain. The parahippocampal place area seems to encode viewpoint-dependent representations, whereas the retrosplenial cortex appears to encode space at a more global level.74 Interestingly, both systems are active during spatial navigation and might represent two anatomically and functionally distinct systems supporting complementary roles in human navigation. Updating one’s own position in the environment also allows one to recover the spatial position of objects with respect to one another.75,76 For an observer O, localizing the position of an invisible object A, having available another visible object B, consists in perceiving direction and distance with respect to B (self-to-object vector, OB) and determining direction and distance of A with respect to B (object-to-object relationship, AB), so that the vector sum can provide the required self-toobject vector, OA.15 Again, object-to-object spatial relationships seem to be encoded primarily as a result Volume 3, November/December 2012

of self-centered views, up to the point that recognition times of interobject distances across different points of view reflect the angular differences between views.77 Constellations of landmarks, however, may aid in the retrieval of an unmarked position, because each of the landmarks bears a specific direction and distance to that position, and the configuration establishes a frame of reference. In a virtual environment experiment in which subjects could make use of multiple landmarks to localize a place, the landmark configuration was altered after training. Subjects had to keep searching for the same place but could only count on the spatial information offered by the altered configuration: the information most used for this localization task was interlandmark distance information rather than interlandmark angular information.78 The recent introduction of virtual reality in experimental psychology laboratories is offering an unprecedented possibility of assessing human spatial cognition in environments that could hardly be realized in the real world,79 with the added value of making it possible to compare human data with results obtained in paradigms typically employed with nonhuman species.80 However, although the space perceived in virtual reality does not offer the same finegrained control over visual cues and their interaction with motor and proprioceptive information, many applications nowadays allow for the construction of fully immersive 3D environments with feedback control, and transfer studies have shown that what is learned in virtual experience can be easily transferred to real-world situations.81–83

Working Memory and Spatial Strategies Many authors84,85 pointed out that the processes of human spatial cognition should be differentiated according to the scale of space taken into consideration (the space of object representation, that of views containing multiple objects, and that of environments that can be experienced only as a series of successive views), and it appears rather likely that despite the commonality of geometric principles that underlie representations and operations on spatial content at different orders of magnitude, these might entail separate processing mechanisms, especially as regards working memory resources.86 One of the most investigated aspects of human spatial cognition concerns the ability to navigate to a goal making use of spatial elements in the environment in order to compute optimal trajectories: studying these trajectories and their endpoints is a powerful tool that can disclose the nature of memory representations and the use of strategies in humans, also revealing


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high variability in navigational ability.87 Typically, the contribution of working memory during a task can be assessed by asking subjects who perform the task to engage in a variety of secondary tasks, one at a time, each requiring a distinctive type of cognitive resource. The identification of the memory system presumably involved in the main task should emerge from the comparison of the performance patterns observed with the various secondary tasks (i.e., the one producing the most interference should reveal which cognitive resource is involved in the main task). By means of this ‘shadowing’ approach, it was shown that both the spatial and the verbal subsystems of human working memory play a role in the encoding of spatial information, both in real-world88 and in virtual reality89,90 experiments that involved navigation in cities or complex environments. Moreover, the latter also revealed that purely visual interference did not produce any effect on navigation.90 The evidence obtained with shadowing tasks provided clear evidence of the role of working memory in human spatial navigation. The results obtained in the studies on spatial reorientation presented in the previous section were also based on verbal and spatial shadowing tasks, which apparently interfered with the conjoining of geometric and nongeometric information in that particular paradigm.44 Although the role of language in reorientation is still debated,91,92 it seems clear that both verbal and spatial working memory are involved in the computations necessary for representing environmental spatial information in humans. Verbal and spatial types of encoding in memory representation are reminiscent of a major theoretical dispute that shaped the foundations of the whole cognitive sciences, namely the contrast between a propositional and an analog stance in the explanation of mental representations.93 Interestingly, it appears that at least for coding spatial information in complex navigable environments, both stances turn out to be correct choices. This was ascertained not only on grounds of the working memory experiments described above but also because of a much richer story of research on the strategies used by human beings coping with instructions for spatial navigation. A very important dichotomy introduced since many decades to separate two such strategies was already alluded to in the previous section on animal spatial cognition, in the description of the taxon and locale systems.8 The taxon/locale distinction, which also reflects the contrast between egocentric and allocentric frames of references presented in the previous paragraphs, is paralleled by a long-lived debate concerning the primacy, in human spatial 574

representation, between a strategy based on the encoding of elements experienced along a navigation path (the route strategy) and a strategy based on the encoding of elements in the environment as seen from above (the survey strategy).94 This ‘route versus survey’ distinction emerged largely as a result of experiments that compared the accuracy of, among others, spatial localization, distance/direction estimation, and map drawing, following real navigation, map reading, and verbal descriptions.95 Several experiments made use of narratives describing sequences of landmarks encountered from the point of view of a hypothetical observer traveling along a route (including subjective terms describing objects as seen in an egocentric perspective, such as ‘in front’ and ‘at left’) or instead narratives describing spatial information as perceived from a bird’s-eye perspective in a map-like fashion (including geographical terms describing the relationships among salient locations, such as ‘south of’ and ‘eastbound’). It was concluded that descriptions of both types can be used to create mental representations of spatial information, and that both types of information are as efficient as those conveyed by direct experience or via the observation of models of large-scale space, namely maps.88,89,95–97 Importantly, evidence has been gathered that spatial information encoded in one format (i.e., firstperson and view-based) can be transformed into representations in the other format (i.e., map-like) with relatively small costs in efficiency.98 Two veins of investigation that have widened the picture on the human ability to form such spatial representations have proven to be the study of developmental change in spatial cognition, dating back to the work of Piaget and Inhelder99 and extending to current research on the representation of verbal and visuospatial encoding of space in toddlers and infants,44,100,101 and also the study of spatial representation in visually impaired persons.102,103 If language and vision are two main foci of human spatial cognition, it is evident that studying the spatial abilities of preverbal infants and those of blind people can provide us with crucial information.

Categorical and Coordinate Spatial Relations Humans (and presumably other species) can also parse the physical world into spatial classes and concepts. An abstract representation of space could have obvious advantages in communication, because categories can be expressed in symbols that can be exchanged. For example, the category ‘to the left’ identifies as equivalent a whole class of positions and





can be expressed either in verbal language or with pictorial symbols (e.g., an arrow: ←). A qualitative or ‘categorical’ type of spatial information104 is clearly too abstract to be useful in fine motor guidance. Yet, neuropsychological evidence clearly indicates that this type of spatial perception and knowledge is also dependent on the same areas of the brain (e.g., parietal lobes) that are important for other spatial functions in the service of navigation and action.105 One possibility is that a process of modularization has taken place for different types of spatial representations. Kosslyn proposed the existence of two qualitatively different types of spatial representation, each corresponding to a separate brain network.106 One spatial representation is based on a quantitative parsing of space and therefore closely related to that of spatial information in the service of action. This type of representation was called coordinate, because it is derived from representations that provide coordinates for navigating into the environment as well as for performing targeted actions such as reaching, grasping, hitting, throwing, or pointing to something. In contrast, the other hypothesized type of spatial representation, labeled categorical spatial relation, parses space in a qualitative manner. For example, two configurations can be described as ‘one to the left of the other’. Each of the two proposed separate networks also appears to be complementarily lateralized. Thus, the brain can represent in parallel the same spatial layout in at least two separate manners,107 a right hemisphere mode that assesses ‘analog’ spatial relations (e.g., the distance between two objects) and a left hemisphere mode that assesses ‘digital’ spatial relations (e.g., whether two objects are attached to one another or above or below the other). The underlying assumption in the above account is that computing separately the two spatial relations (instead of, for example, taking the quantitative representation and making it coarser by grouping the finer locations) could result in a more efficient representation of space, where both properties can be attended simultaneously. The fact that different types of representation can be processed independently by each hemisphere has been repeatedly confirmed by behavioral methods that use the lateralized (and tachistoscopic) presentation of visual stimuli to normal participants.106,108–110 The perception of categorical and coordinate relations does not typically involve any specific action in space but only observational judgments (e.g., noticing or remembering the position of objects in a display). Thus, the evidence from categorical and coordinate spatial processing (together with the literature on other spatial transformations or operations; e.g., Volume 3, November/December 2012

mental rotations of shapes and visual maze solving) clearly indicates that the two hypothesized networks do merely support not only the ‘act’ function but also two other central functions of visuospatial representations: to ‘know’ and ‘talk’. That is, humans can put into words or verbal propositions (as well as into gestures) any type of spatial relations, whether quantitative (by use of numerical systems, geometric systems specifying angles, and eccentricities) or qualitative (by use of prepositions and locutions). If abstract spatial relations between objects in a visual scene can be effortlessly perceived, these representations are particularly apt to be efficiently coded in a propositional manner (e.g., on-top-of [glass, table]). The evidence for the existence of a division of labor for analog versus digital spatial relations in humans is now clearly established, and local interactions with linguistic and semantic networks may play a key role in the manner in which the spatial system is organized. That is, biasing categorical spatial representations within a left hemisphere’s substrate by ‘yoking’ them with linguistic processes may facilitate a joint operation between perception, language, and thought.106,111

SPACE, BRAINS, AND ROBOTS Data and models on spatial cognition can no longer be taken separately from the huge amount of information that is being accumulated about the involvement of the brain and the role that specialized neurons and dedicated areas and networks play in spatial functions. The interplay of psychology and neuroscience in this respect is extraordinary, not only because psychology provides neuroscience with the behavioral paradigms necessary to carry out the appropriate experiments to tackle specific questions about spatial cognition but also because theoretical inputs coming from the results of tests carried out in psychology laboratories open up novel avenues for hypothesis-driven exploration of brain functions, and the same happens in the opposite direction, from neuroscience to psychology. Other overview articles in this journal deal with specific aspects of the neural bases of spatial cognition, as is expected by the importance and vastness of the field. It might suffice to remember that among the types of single cells that were discovered in rodent electrophysiology, not a few have turned out to be specialized for spatial functions. Place cells (whose property is that of firing selectively when an animal dwells by one specific location in the environment) being certainly the progenitor type in this fortunate history,112 one could also mention head-direction cells (active when the animal’s head assumes a specific orientation, disregarding of the animal’s position in the environment),113 grid


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cells (active when the animal dwells by one of many locations over the environment, according to a Cartesian grid structure),114 and border cells (active when the animal is in the vicinity of a border or wall).115 This list of selective cells makes it clear how evolution endowed brains with extremely specialized machinery to process spatial content. The investigation of cell and connection properties by anatomy and histology, the elucidation of brain regions involved in spatial processing by means of lesion studies in animals and humans, and more recently the adoption of neuroimaging techniques to assess directly the activation (as well as the connectivity) of those brain regions as subjects perform spatial tasks are revealing how the ‘spatial brain’ makes spatial cognition possible. As the proposal was made of equating the hippocampus with the cognitive map of space,8 research on the role of the hippocampal formation and the surrounding brain regions has progressed astonishingly,116 branching also in the direction of other brain regions involved in spatial mapping,117 and promises to keep offering newer and newer insights. If psychology and neuroscience ‘play together’ in the search for the bases of spatial cognition, one could say that the relationship of robotics and cognitive engineering to the psychology (and the neuroscience) of spatial cognition118 is more unidirectional (although see Ref 119 for a view suggesting more reciprocal interaction). In their own words, robot and autonomous agent designers are predominantly inspired by the results and models provided by empirical research on the spatial abilities of living organisms, in order to design artificial agents and mobile robots that gather sensory information, react in an adaptive manner, and possibly form long-lasting representations of spatial aspects of the surrounding environment. This ‘biomimetic approach’ aims at transferring knowledge obtained about biological navigation and spatial cognition to the implementation of technical applications and is clearly motivated to exploit the most biologically plausible solutions. It must be remarked that, given the fact that engineering aims at designing the best solution to a problem and that there might be many nonbiologically plausible solutions to the problem of representing space for robot navigation, subscribing to a biological perspective is probably based on the confidence arising from the fact that biological solutions are those that have passed the hardest test, that of evolution.

CONCLUSION Spatial cognition can be seen as the set of mental representations and processes evolved in living 576

organisms to cope with the physical dimension of space. It is a basic psychological function that assists in performing behaviors, planning movements, and evaluating events in the environment. It allows animals not only to compute positions with respect to themselves but also to compute positions relative to each other. Research in animals and humans has shed light on the mechanisms involved in the storing and active use of spatial information that are especially relevant for navigation and also for forming and manipulating abstract spatial representations. Laboratory experiments and field research in animals, from invertebrates to primates, focused on the role of landmarks in spatial orientation and on the mechanisms based on the encoding of distance and direction or on the matching of stored views or snapshots. An entire research line initiated with studies on animals, moreover, confirmed the importance of spatial representations based on the geometry of extended surfaces and their interaction with nongeometric information derived from landmarks. The vivacity in this line of research boosted the cross-talk among experimental, developmental, and comparative psychology over the idea of a primacy of geometry in spatial cognition, although results are inconclusive as regards the modularity of geometric information, and much else about this topic will have to be understood in the years to come. Research focusing on humans provided important results on the role of frames of reference in the formation of spatial representations. Experimental work carried out in real environments, but also using virtual reality and neuroimaging, supports the coexistence (albeit with different weights) of observercentered views and observer-independent mappings of the external world, the former type of frame of reference being exploited more ubiquitously than the latter. Moreover, experiments on real-world navigation and abstract mapping allowed to clearly distinguish the relative contribution of verbal and spatial working memory components in forming spatial representations and showed the recourse to two different strategies in encoding spatial information (‘route’ vs ‘survey’). Finally, at the more abstract level of human categorization, it has been shown that alongside the quantitative, fine-grained processing of spatial information, useful for navigation and action control (coordinate spatial relations), a qualitative processing of spatial information, parsing continuous space into separate regions, is used for describing spatial relations by means of referential communication (categorical spatial relations). The liveliness of current research on spatial cognition in psychology is interlinked to the incredible





growth of research on spatial cognition in the neurosciences as well as to the constant search for ingenious solutions to the problem of representing (and coping

with) space in robotics. The success of such a joint effort probably makes spatial cognition one of the most representative fields of the cognitive sciences.

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FURTHER READING Dolins FR, Mitchell RW, eds. Spatial Perception, Spatial Cognition: Mapping the Self and Space. Cambridge: Cambridge University Press; 2010. Allen GL, ed. Human Spatial Memory: Remembering Where. Hillsdale: Erlbaum; 2004. Derdikman D, Moser EI. A manifold of spatial maps in the brain. Trends Cogn Sci 2010, 14:561–569.

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Neurology as a Dialectical Synthesis of Faculty Psychology.

Forward and backward inference in spatial cognition.

Vision, spatial cognition and intellectual disability.

Cerebellum and spatial cognition in goldfish.

Spatial cognition: a tabula rasa for the sense of direction.

Spatial cognition in Alzheimer's disease: subtypes of global-local impairment.

Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.

Cognition and the compassion deficit: the social psychology of helping behaviour in nursing.

Going with the Grain of Cognition: Applying Insights from Psychology to Build Support for Childhood Vaccination.

Spatial associations in numerical cognition--from single digits to arithmetic.

Balance training improves memory and spatial cognition in healthy adults.

Primate spatial strategies and cognition: introduction to this special issue.

Sex differences in spatial cognition: advancing the conversation.

Introduction to the topic on modeling spatial cognition.

Self-locomotion and spatial language and spatial cognition: insights from typical and atypical development.

Where am I? Who am I? The Relation Between Spatial Cognition, Social Cognition and Individual Differences in the Built Environment.

The cultural psychology of Kohut's self psychology.

Effect of nebracetam on the disruption of spatial cognition in rats.

The effect of childhood trauma on spatial cognition in adults: a possible role of sex.

Attention and spatial cognition: Neural and anatomical substrates of visual neglect.

Thinking about quantity: the intertwined development of spatial and numerical cognition.

6 Mice Spatial Cognition.

Estrogen receptor α functions in the regulation of motivation and spatial cognition in young male rats.

Exploring the functional advantages of spatial and visual cognition from an architectural perspective.