Allocentric Spatial Representations Research Articles

When do objects become landmarks? A VR study of the effect of task relevance on spatial memory.

We investigated how objects come to serve as landmarks in spatial memory, and more specifically how they form part of an allocentric cognitive map. Participants performing a virtual driving task incidentally learned the layout of a virtual town and locations of objects in that town. They were subsequently tested on their spatial and recognition memory for the objects. To assess whether the objects were encoded allocentrically we examined pointing consistency across tested viewpoints. In three experiments, we found that spatial memory for objects at navigationally relevant locations was more consistent across tested viewpoints, particularly when participants had more limited experience of the environment. When participants’ attention was focused on the appearance of objects, the navigational relevance effect was eliminated, whereas when their attention was focused on objects’ locations, this effect was enhanced, supporting the hypothesis that when objects are processed in the service of navigation, rather than merely being viewed as objects, they engage qualitatively distinct attentional systems and are incorporated into an allocentric spatial representation. The results are consistent with evidence from the neuroimaging literature that when objects are relevant to navigation, they not only engage the ventral “object processing stream”, but also the dorsal stream and medial temporal lobe memory system classically associated with allocentric spatial memory.

Human neural systems underlying rigid and flexible forms of allocentric spatial representation

Previous studies suggest the importance of medial temporal lobe, areas of parietal cortex, and retrosplenial cortex in human spatial navigation, though the exact role of these structures in representing the relations of elements within a spatial layout ("allocentric" representation) remains unresolved. Hippocampal involvement, in particular, during memory processing is affected by whether a previously formed representation is employed in a novel fashion ("flexible" usage) or in a manner comparable with how it was encoded originally ("rigid" usage). To address whether brain systems are differentially involved during flexible vs. rigid utilization of a pre-existing allocentric representation, subjects encoded the position of six different target buildings relative to a centrally located landmark building in a virtual city seen from an aerial view. They then actively searched for the locations of these target buildings using the landmark (rigid retrieval) or using a previously shown target building in a novel fashion (flexible retrieval) while undergoing fMRI. Activations in posterior superior parietal cortex and precuneus were greater during more rigid than flexible forms of allocentric retrieval while activation in the hippocampus decreased linearly over blocks during flexible allocentric retrieval. A functional connectivity analysis further revealed significant interactions between hippocampus and these parietal areas during flexible compared with rigid allocentric retrieval. These results extend previous models of the neural basis of spatial navigation by suggesting that while the posterior superior parietal cortex/precuneus play an important role in allocentric representation, the hippocampus, and interactions between hippocampus and these parietal areas, are important for flexible utilization of these representations.

The hippocampus and spatial constraints on mental imagery

We review a model of imagery and memory retrieval based on allocentric spatial representation by place cells and boundary vector cells (BVCs) in the medial temporal lobe, and their translation into egocentric images in retrosplenial and parietal areas. In this model, the activity of place cells constrain the contents of imagery and retrieval to be coherent and consistent with the subject occupying a single location, while the activity of head-direction cells along Papez's circuit determine the viewpoint direction for which the egocentric image is generated. An extension of this model is discussed in which a role for grid cells in dynamic updating of representations (mental navigation) is included. We also discuss the extension of this model to implement a version of the dual representation theory of post-traumatic stress disorder (PTSD) in which PTSD arises from an imbalance between weak allocentric hippocampal-mediated contextual representations and strong affective/sensory representations. The implications of these models for behavioral, neuropsychological, and neuroimaging data in humans are explored.

Neural Encoding of Objects Relevant for Navigation and Resting State Correlations with Navigational Ability

Objects along a route can help us to successfully navigate through our surroundings. Previous neuroimaging research has shown that the parahippocampal gyrus (PHG) distinguishes between objects that were previously encountered at navigationally relevant locations (decision points) and irrelevant locations (nondecision points) during simple object recognition. This study aimed at unraveling how this neural marking of objects relevant for navigation is established during learning and postlearning rest. Twenty-four participants were scanned using fMRI while they were viewing a route through a virtual environment. Eye movements were measured, and brain responses were time-locked to viewing each object. The PHG showed increased responses to decision point objects compared with nondecision point objects during route learning. We compared functional connectivity between the PHG and the rest of the brain in a resting state scan postlearning with such a scan prelearning. Results show that functional connectivity between the PHG and the hippocampus is positively related to participants' self-reported navigational ability. On the other hand, connectivity with the caudate nucleus correlated negatively with navigational ability. These results are in line with a distinction between egocentric and allocentric spatial representations in the caudate nucleus and the hippocampus, respectively. Our results thus suggest a relation between navigational ability and a neural preference for a specific type of spatial representation. Together, these results show that the PHG is immediately involved in the encoding of navigationally relevant object information. Furthermore, they provide insight into the neural correlates of individual differences in spatial ability.

Unimanual SNARC Effect: Hand Matters

A structural representation of the hand embedding information about the identity and relative position of fingers is necessary to counting routines. It may also support associations between numbers and allocentric spatial codes that predictably interact with other known numerical spatial representations, such as the mental number line (MNL). In this study, 48 Western participants whose typical counting routine proceeded from thumb-to-little on both hands performed magnitude and parity binary judgments. Response keys were pressed either with the right index and middle fingers or with the left index and middle fingers in separate blocks. 24 participants responded with either hands in prone posture (i.e., palm down) and 24 participants responded with either hands in supine (i.e., palm up) posture. When hands were in prone posture, the counting direction of the left hand conflicted with the direction of the left–right MNL, whereas the counting direction of the right hand was consistent with it. When hands were in supine posture, the opposite was true. If systematic associations existed between relative number magnitude and an allocentric spatial representation of the finger series within each hand, as predicted on the basis of counting habits, interactions would be expected between hand posture and a unimanual version of the spatial–numerical association of response codes (SNARC) effect. Data revealed that with hands in prone posture a unimanual SNARC effect was present for the right hand, and with hands in supine posture a unimanual SNARC effect was present for the left hand. We propose that a posture-invariant body structural representation of the finger series provides a relevant frame of reference, a within-hand directional vector, that is associated to simple number processing. Such frame of reference can significantly interact with stimulus–response correspondence effects, like the SNARC, that have been typically attributed to the mapping of numbers on a left-to-right mental line.

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

The hippocampus is crucial for both spatial navigation and episodic memory, suggesting that it provides a common function to both. Here we adapt a spatial paradigm, developed for rodents, for use with functional MRI in humans to show that activation of the right hippocampus predicts the use of an allocentric spatial representation, and activation of the left hippocampus predicts the use of a sequential egocentric representation. Both representations can be identified in hippocampal activity before their effect on behavior at subsequent choice-points. Our results suggest that, rather than providing a single common function, the two hippocampi provide complementary representations for navigation, concerning places on the right and temporal sequences on the left, both of which likely contribute to different aspects of episodic memory.

The dynamic process of cognitive mapping in the absence of visual cues:human data compared with animal studies

The present study aimed to investigate the behavior involved in constructing spatial representation in humans. For this, blindfolded adult human subjects were introduced into an unfamiliar environment, where they were requested to move incessantly for 10 min. Analysis of the locomotor activity of the participants revealed the following exploratory behaviors: (1) ;looping'; (2) ;wall-following'; (3) ;step-counting'; (4) ;cross-cutting'; and (5) ;free traveling'. Looping is a typical exploratory mode of sightless explorers, based on returning to a recently traveled place. Wall-following is common in enclosed spaces, whereby explorers follow the perimeter of the environment. Both looping and wall-following are based on an egocentric frame of reference by which explorers obtain information about the shape, size and landmarks in the environment. Blindfolded explorers displayed step-counting in order to scale the environment and the relationships in it. Altogether, exploration by looping, wall-following and step-counting resulted in an allocentric spatial representation. The acquisition of spatial representation was manifested by cross-cutting and free travel, with subjects walking in a relatively fast and decisive manner. In light of the above modes of activity, we suggest that exploration of an unfamiliar environment is a synergetic self-organized process (synergetic inter-representation networks, SIRN model); an interplay between external and internal representations. According to this model, the interplay gives rise to an order parameter, such as the environment's dimensions or geometry, enabling progression to a subsequent exploratory behavior. This dynamic and sequential interplay reaches a steady state when a spatial representation (i.e. ;cognitive map') is established.

Memory for familiar environments learned in the remote past: fMRI studies of healthy people and an amnesic person with extensive bilateral hippocampal lesions

Preserved remote spatial memory in amnesic people with bilateral hippocampal damage, including the well-studied case K.C., challenges spatial theories, which assume that the hippocampus is needed to support all allocentric spatial representations, old or new. It remains possible, however, that residual hippocampal tissue is functional and contributes to successful performance. Here, we examine brain activity with fMRI during the retrieval of spatial information in K.C. and in healthy controls using landmark and route stimuli from a premorbidly familiar neighborhood that K.C. can navigate normally. In all participants, activity was found in the parahippocampal cortex, but not in the hippocampus itself, during all navigational tasks on which K.C. performs well, even though part of his hippocampus remains viable. The opposite pattern was observed on a house recognition task, which is inconsequential to navigation, and on which K.C. performed poorly. On that task, K.C. recruited the right hippocampus presumably because even "familiar" houses were treated as novel by him, whereas controls recruited occipitotemporal cortex, including parahippocampal cortex. The distinction between recent and remote memory, therefore, may apply as much to spatial theories of hippocampal function as it does to theories emphasizing the role of the hippocampus in other types of explicit memory.

Topographical, Autobiographical and Semantic Memory in a Patient with Bilateral Mesial Temporal and Retrosplenial Infarction

According to Consolidation Theory (Squire, 1992, Psychological Review, 99, 195; Squire & Alvarez, 1995, Current Opinion in Neurobiology, 5, 169), the mesial temporal lobes have a time-limited role in the maintenance, storage and retrieval of retrograde declarative memories, such that they are not necessary for recalling remote memories. In contrast, proponents of the Multiple Trace Theory (Fuji, Moscovitch, & Nadel, 2000, Handbook of neuropsychology, 2nd ed., p 223, Amsterdam, New York: Elsevier; Nadel & Moscovitch, 1999, Current Opinion in Neurobiology, 7, 217) posit that the mesial temporal lobe (MTL) is necessary for remembering detailed autobiographical and topographical material from all time periods. A third theory of hippocampal function, the Cognitive Map Theory (O'Keefe & Nadel, 1978, The hippocampus as a cognitive map. Oxford: Clarendon), states that the hippocampus is involved in the processing of allocentric spatial representations. The precise role of the MTL in remote memory has been difficult to elucidate, as the majority of studies present cases with widespread brain damage that often occurred many years prior to testing. We investigated retrograde autobiographical, semantic and topographical memories in a subject (SG) who had recently sustained infarctions confined to the MTL and retrosplenial region bilaterally. Inconsistent with the predictions of Cognitive Map Theory, memory for spatial maps that were learned in the past was preserved. Additional testing indicated that SG suffered from a landmark agnosia, which affected remotely and recently acquired information equally. SG was also poor at imagining which direction he would have to turn his body to move from one landmark to another. In accordance with Consolidation Theory, SG performed similarly to control subjects for remote time periods on various measures of retrograde autobiographical memory and demonstrated intact knowledge regarding famous faces and vocabulary terms that were acquired in the past. In contrast, memory for remote public events was impaired. The current findings indicate that the mesial temporal and/or retrosplenial regions have little role to play in memory for remotely acquired spatial maps, autobiographical memories, famous faces or vocabulary terms. However, the findings for landmark naming, directional calculations between landmarks and knowledge of public events suggest that the MTL and/or retrosplenial cortices remain important for accessing these types of memories indefinitely.

Conceptuality in Spatial Representations

The notion of conceptuality is still unclear and vague. I will present a definition of conceptual and nonconceptual representations that is grounded in different aspects of the representations’ structures. This definition is then used to interpret empirical results from human and animal navigation. It will be shown, that the distinction between egocentric and allocentric spatial representations can be matched onto the conceptual vs. nonconceptual distinction. The phenomena discussed in spatial navigation are thereby put into a wider context of cognitive abilities, which allows for new explanations of certain features of spatial representations and how they are linked to other capacities, like perception and reasoning.

Finding your way in the world: on the neurocognitive basis of spatial memory and orientation in humans

Finding your way home, remembering where you left the car keys or directing someone to the nearest hospital are examples of highly complex cognitive tasks based on spatial memory and orientation. Without these functions, navigating through daily life would be impossible. Our ability to construct spatial representations of the outside world, and to store them in our memory is likely to underlie many other higher cognitive functions in humans, such as decision-making and planning. Many other animals possess the ability to navigate around their environment but there are certain higher-order features of the human system, such as the ability to communicate spatial information verbally or the ability to switch perspectives, which are uniquely human. This symposium will address how the variety of spatial memory processes is implemented in the human brain, and how it is characterized by differences across species, and within the human species (such as in gender, age and clinical populations). We will start with sketching an evolutionary taxonomy of spatial memory and spatial representations. Next, we will discuss how (certain) spatial abilities might develop during the human ontogeny. An important question of course is how the human brain carries out mental activities such as navigation and perspective taking. We will illustrate this by examples of recent neuroimaging studies on allocentric spatial representations and perspective switches. More insight in to how the human brain deals with spatial information processing can be gathered from neurological cases in which spatial neurological circuits are affected. Another way to understand how spatial representations of the surrounding world are created comes from studying situations in which the sensory input channels are limited, such as in the case of blindness. This sheds light on the supposed supramodality of spatial representations. Finally, the versatility of the human spatial memory system will be illustrated by a closer look at individual differences in humans: how do men and women differ in spatial memory ability?. This symposium derives from a EU funded NEST PATHFINDER research initiative (see http://www.wayfinding.fss.uu.nl/).

Hippocampal Lesion Prevents Spatial Relational Learning in Adult Macaque Monkeys

The role of the hippocampus in spatial learning and memory has been extensively studied in rodents. Comparable studies in nonhuman primates, however, are few, and findings are often contradictory. This may be attributable to the failure to distinguish between allocentric and egocentric spatial representations in experimental designs. For this experiment, six adult monkeys received bilateral hippocampal ibotenic acid lesions, and six control subjects underwent sham surgery. Freely moving monkeys then foraged for food located in two arrays of three distinct locations among 18 locations distributed in an open-field arena. Multiple goals and four pseudorandomly chosen entrance points precluded the monkeys' ability to rely on an egocentric strategy to identify food locations. Monkeys were tested in two conditions. First, local visual cues marked the food locations. Second, no local cues marked the food locations, so that monkeys had to rely on an allocentric (spatial relational) representation of the environment to discriminate these locations. Both hippocampal-lesioned and control monkeys discriminated the food locations in the presence of local cues. However, in the absence of local cues, control subjects discriminated the food locations, whereas hippocampal-lesioned monkeys were unable to do so. Interestingly, histological analysis of the brain of one control monkey whose behavior was identical to that of the experimentally lesioned animals revealed a bilateral ischemic lesion restricted to the hippocampus. These findings demonstrate that the adult monkey hippocampal formation is critical for the establishment or use of allocentric spatial representations and that selective damage of the hippocampus prevents spatial relational learning in adult nonhuman primates.

Roles of egocentric and allocentric spatial representations in locomotion and reorientation.

Four experiments investigated the nature of spatial representations used in locomotion. Participants learned the layout of several objects and then pointed to the objects while blindfolded in 3 conditions: before turning (baseline), after turning to a new heading (updating), and after disorientation (disorientation). The internal consistency of pointing in the disorientation condition was relatively high and equivalent to that in the baseline and updating conditions, when the layout had salient intrinsic axes and the participants learned the locations of the objects on the periphery of the layout. The internal consistency of pointing was disrupted by disorientation when participants learned the locations of objects while standing amid them and the layout did not have salient intrinsic axes. It was also observed that many participants retrieved spatial relations after disorientation from the original learning heading. These results indicate that people form an allocentric representation of object-to-object spatial relations when they learn the layout of a novel environment and use that representation to locate objects around them. Egocentric representations may be used to locate objects when allocentric representations are not of high fidelity.

Egocentric and allocentric spatial memory in idiopathic cervical dystonia

To investigate whether impaired spatial memory contributes to cognitive deficits in idiopathic cervical dystonia (ICD). The authors tested 16 untreated patients with ICD and 16 healthy controls with four variants of a classic spatial memory task, in which subjects were requested to recall the locations of 16 toy objects either immediately after their presentation or after an unfilled delay of 10 minutes. By varying the spatial relationship between subject and toy object array, we tested encoding and memory of spatial relationships between subject and toy objects (egocentric tasks) and of spatial relationships between toy objects and environment (allocentric tasks). In all four tasks, absolute performance of patients did not differ significantly from controls, suggesting that there are no significant spatial memory deficits in ICD. However, significant correlations between egocentric and allocentric task performance were found in patients but not in controls. While control subjects flexibly used egocentric or allocentric spatial representations in memory tasks, patients with idiopathic cervical dystonia (ICD) solved both task types with a single allocentric strategy. Our findings point to the existence of compensatory mechanisms between distinct neural systems supporting egocentric and allocentric spatial representations in ICD.

Allocentric and Egocentric Spatial Impairments in a Case of Topographical Disorientation

We describe a patient with a topographical disorientation after a stroke of the right mediotemporooccipital lobe including the parahippocampal cortex (PHC). Clinical observations and neuropsychological testing reveal an impairment of allocentric spatial representations as well as impairments of visuospatial learning and memory. These findings are in accordance with the well-known function of the PHC in topographical disorientation. As a new finding, results from oculomotor tasks show additional impairments of the egocentric spatial coordinate frame suggesting that in topographical disorientation due to a lesion of the right mediotemporooccipital lobe not only allocentric but also egocentric visuospatial functions are disturbed.

Spatial representation in the entorhinal cortex.

As the interface between hippocampus and neocortex, the entorhinal cortex is likely to play a pivotal role in memory. To determine how information is represented in this area, we measured spatial modulation of neural activity in layers of medial entorhinal cortex projecting to the hippocampus. Close to the postrhinal-entorhinal border, entorhinal neurons had stable and discrete multipeaked place fields, predicting the rat's location as accurately as place cells in the hippocampus. Precise positional modulation was not observed more ventromedially in the entorhinal cortex or upstream in the postrhinal cortex, suggesting that sensory input is transformed into durable allocentric spatial representations internally in the dorsocaudal medial entorhinal cortex.

Object localisation and frames of reference

In this paper, we explore which spatial frames of reference, egocentric or allocentric, are used to locate objects either in relation to ourselves (i.e. subject-to-object localisation) or to other objects (i.e. object-to-object localisation). In particular, we wanted to know whether the same or different frames of reference are used in these two different kinds of localisation after learning the environment in an egocentric way. Egocentric frames of reference are determined by the position of the person in relation to the spatial layout, whereas allocentric frames of reference are centred on the environment or on objects, independent of a person’s position. We hypothesised that subject-to-object localisation is based on egocentric spatial representations, whereas object-to-object localisation is based on allocentric spatial representations. Participants were asked to study eight common objects, placed in a circle. Next, half of the participants had to point to an object in relation to their imagined position (egocentric condition) and the other half to an object in relation to another object (allocentric condition). The overall results show no difference between subject-to-object and object-to-object localisation. In both cases, access to positions corresponding to the front/back body axis was facilitated, in terms of both latency and error. Moreover, participants were able to retrieve objects’ positions better from the perspective from which they had learned the spatial array than from new perspectives. These results support the conclusion that egocentric coordinates, which are selected on the basis of our body-centred experience of the environment, define spatial representations underlying both subject-to-object and object-to-object localisation.

Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation

Rats with dorsal hippocampus or associative parietal cortex (APC) lesions and sham-operated controls were trained on variants of the Morris water maze navigation task. In the ‘proximal landmark condition’, the rats had to localize the hidden platform solely on the basis of three salient object landmarks placed directly in the swimming pool. In the ‘distal landmark condition’, rats could rely only on distal landmarks (room cues) to locate the platform. In the ‘beacon condition’, the platform location was signaled by a salient cue directly attached to it. Rats with hippocampal lesions were impaired in the distal and to a less extent in the proximal landmark condition whereas rats with parietal lesions were impaired only in the proximal landmark condition. None of the lesioned groups was impaired in the beacon condition. These results suggest that the processing of information related to proximal, distal landmarks or associated beacon are mediated by different neural systems. The hippocampus would contribute to both proximal and distal landmark processing whereas the APC would be involved in the processing of proximal landmarks only. Navigation relying on a cued-platform would not require participation of the hippocampus nor the APC. Assuming that the processing of proximal landmarks heavily depends on the integration of visuospatial and idiothetic information, these results are consistent with the hypothesis that the APC plays a role in the combination of multiple sensory information and contributes to the formation of an allocentric spatial representation.

Functional role of rat prelimbic-infralimbic cortices in spatial memory: evidence for their involvement in attention and behavioural flexibility

The involvement of the medial prefrontal cortex (mPFC), and more particularly the prelimbic and infralimbic cortices (PL-IL area), in spatial memory remains controversial. The present study investigates the effects of neurotoxic lesions restricted to the PL-IL area of the mPFC in rats trained in two different spatial tasks. In experiment 1, PL-IL lesioned rats showed normal acquisition of a delayed non-matching to position task. They were also able to plan their responses for a prospective strategy but were transiently disrupted when the initial delay was extended. In experiment 2, rats were trained to locate one baited box among 13 identical boxes distributed on a circular arena. Lesioned rats performed normally when trained from a single start position but were severely disrupted when four start positions were used. A probe trial showed this deficit was not due to failure to learn the goal location. The addition of a proximal cue signalling the goal box helped lesioned rats to directly open the goal box, but did not compensate for greater distances that they travelled to reach it. Results from both experiments indicate that the PL-IL area is directly involved neither in allocentric spatial representations nor prospective memory and is not specifically involved in working memory. This area seems more likely to be involved in both attentional processes and behavioural flexibility that may be important for processing information for working memory as well as for spatial memory.

Self, World and Space: The Meaning and Mechanismsof Ego- and Allocentric Spatial Representation

The problem of how physical systems, such as brains, come to representthemselves as subjects in an objective world is addressed. I developan account of the requirements for this ability that draws on and refines work in a philosophical tradition that runs from Kant throughPeter Strawson to Gareth Evans. The basic idea is that the ability torepresent oneself as a subject in a world whose existence isindependent of oneself involves the ability to represent space, andin particular, to represent oneself as one object among others in anobjective spatial realm. In parallel, I provide an account of howthis ability, and the mechanisms that support it, are realizedneurobiologically. This aspect of the article draws on, and refines,work done in the neurobiology and psychology of egocentric andallocentric spatial representation.