Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies

At least two main cognitive strategies can be used to solve a complex navigation task: the allocentric or map‐based strategy and the sequential egocentric or route‐based strategy. The sequential egocentric strategy differs from a succession of independent simple egocentric responses as it requires a sequential ordering of events, possibly sharing functional similarity with episodic memory in this regard. To question the possible simultaneous encoding of sequential egocentric and allocentric strategies, we developed a paradigm in which these two strategies are spontaneously used or imposed. Our results evidenced that sequential egocentric strategy can be spontaneously acquired at the onset of the training as well as allocentric strategy. Allocentric and sequential egocentric strategies could be used together within a trial, and bidirectional shifts (between trials) were spontaneously performed during the training period by 30% of the participants. Regardless of the strategy used spontaneously during the training, all participants could execute immediate shifts to the opposite non previously used strategy when this strategy was imposed. Altogether, our findings suggest that subjects acquire different types of spatial knowledge in parallel, namely knowledge permitting allocentric navigation as well as knowledge permitting sequential egocentric navigation. © 2009 Wiley‐Liss, Inc.     

Time course of allocentric decay, egocentric decay, and allocentric-to-egocentric conversion in memory-guided reach

Allocentric cues can be used to encode locations in visuospatial memory, but it is not known how and when these representations are converted into egocentric commands for behaviour. Here, we tested the influence of different memory intervals on reach performance toward targets defined in either egocentric or allocentric coordinates, and then compared this to performance in a task where subjects were implicitly free to choose when to convert from allocentric to egocentric representations. Reach and eye positions were measured using Optotrak and Eyelink Systems, respectively, in fourteen subjects. Our results confirm that egocentric representations degrade over a delay of several seconds, whereas allocentric representations remained relatively stable over the same time scale. Moreover, when subjects were free to choose, they converted allocentric representations into egocentric representations as soon as possible, despite the apparent cost in reach precision in our experimental paradigm. This suggests that humans convert allocentric representations into egocentric commands at the first opportunity, perhaps to optimize motor noise and movement timing in real-world conditions.     

A comparison of egocentric and allocentric spatial memory in medial temporal lobe and Korsakoff amnesics

Two patients with medial temporal lobe damage, seven Korsakoff amnesics and fourteen healthy control subjects were tested on three conditions of a spatial memory test ('short delay', 'allocentric' and 'egocentric'). The task required subjects to recall the position of a single spot of light presented on a board after various delays. The 'short delay' condition tested memory over very short, unfilled intervals. The other two conditions used longer, filled delays. The allocentric condition required subjects to move to a different place around the board before recalling the position of the light. In the egocentric condition stimuli were presented in darkness, which eliminated allocentric cues. The Korsakoff amnesics were impaired at all delays of the short delay tasks, suggesting poor encoding. On the allocentric and egocentric tasks the Korsakoff amnesics showed a comparable impairment in the two conditions, which worsened with delay. This accelerated forgetting suggested that the Korsakoff amnesics also had impaired memory for allocentric and egocentric information. The patients with medial temporal lobe damage were unimpaired in the 'short delay' condition suggesting intact encoding and short-term memory of spatial information. However, they were impaired in the allocentric condition and showed accelerated loss of allocentric spatial information. In the egocentric condition, while the performance of one patient was impaired, the performance of the other was as good as controls. This result suggests that, in contrast to allocentric spatial memory, which is sensitive to medial temporal lobe damage, an intact medial temporal lobe need not be necessary for successful performance on an egocentric spatial memory task.     

Learning associations between places and visual cues without learning to navigate: neither fornix nor entorhinal cortex is required

Rats with fornix transection, or with cytotoxic retrohippocampal lesions that removed entorhinal cortex plus ventral subiculum, performed a task that permits incidental learning about either allocentric (Allo) or egocentric (Ego) spatial cues without the need to navigate by them. Rats learned eight visual discriminations among computer-displayed scenes in a Y-maze, using the constant-negative paradigm. Every discrimination problem included two familiar scenes (constants) and many less familiar scenes (variables). On each trial, the rats chose between a constant and a variable scene, with the choice of the variable rewarded. In six problems, the two constant scenes had correlated spatial properties, either Allo (each constant appeared always in the same maze arm) or Ego (each constant always appeared in a fixed direction from the start arm) or both (Allo + Ego). In two No-Cue (NC) problems, the two constants appeared in randomly determined arms and directions. Intact rats learn problems with an added Allo or Ego cue faster than NC problems; this facilitation provides indirect evidence that they learn the associations between scenes and spatial cues, even though that is not required for problem solution. Fornix and retrohippocampal-lesioned groups learned NC problems at a similar rate to sham-operated controls and showed as much facilitation of learning by added spatial cues as did the controls; therefore, both lesion groups must have encoded the spatial cues and have incidentally learned their associations with particular constant scenes. Similar facilitation was seen in subgroups that had short or long prior experience with the apparatus and task. Therefore, neither major hippocampal input-output system is crucial for learning about allocentric or egocentric cues in this paradigm, which does not require rats to control their choices or navigation directly by spatial cues.     

A comparison of egocentric and allocentric age-dependent spatial learning in the beagle dog

Spatial discriminations can be performed using either egocentric information based on body position or allocentric information based on the position of landmarks in the environment. Beagle dogs ranging from 2 to 16 years of age were tested for their ability to learn a novel egocentric spatial discrimination task that used two identical blocks paired in three possible spatial positions (i.e. left, center and right). Dogs were rewarded for responding to an object furthest to either their left or right side. Therefore, when the center location was used, it was correct on half of the trials and incorrect on the other half. Upon successful acquisition of the task, the reward contingencies were reversed, and the dogs were rewarded for responding to the opposite side. A subset of dogs was also tested on an allocentric spatial discrimination task, landmark discrimination. Egocentric spatial reversal learning and allocentric discrimination learning both showed a significant age-dependent decline, while initial egocentric learning appeared to be age-insensitive. Intra-subject correlation analyses revealed a significant relationship between egocentric reversal learning and allocentric learning. However, the correlation only accounted for a small proportion of the variance, suggesting that although there might be some common mechanism underlying acquisition of the two tasks, additional unique neural substrates were involved depending on whether allocentric or egocentric spatial information processing was required.     

Idiosyncratic orientation strategies influence self-controlled whole-body rotations in the dark

The present experiment examined the influence of spatial orientation strategies on human subjects' accuracy in a self-controlled whole-body rotation task in the dark. Subjects were seated on a robotic chair and had to perform 360 degrees rotations with or without the presentation of a space-fixed target. Performance was compared between subjects who preferably used an "egocentric" or an "allocentric" strategy. Results suggest that orientation strategies might be tightly linked to sensory integration processes.     

Topographical disorientation in a patient with late-onset blindness with multiple acute ischemic brain lesions

The neurological basis for topographical disorientation has recently shifted from a model of navigation utilizing egocentric techniques alone, to multiple parallel systems of topographical cognition including egocentric and allocentric strategies. We explored if this hypothesis may be applicable to a patient with late-onset blindness. A 72-year-old male with bilateral blindness experienced a sudden inability to navigate after suffering a stroke. Multiple lesions scattered bilaterally throughout the parietal-occipital lobes were found. Deficits in the neural correlates underlying egocentric or allocentric strategies may result in topographical disorientation, even if one appears to be the predominant orientation strategy utilized.     

Asymmetric Influence of Egocentric Representation onto Allocentric Perception

Objects in the visual world can be represented in both egocentric and allocentric coordinates. Previous studies have found that allocentric representation can affect the accuracy of spatial judgment relative to an egocentric frame, but not vice versa. Here we asked whether egocentric representation influenced the processing speed of allocentric perception. We measured the manual reaction time of human subjects in a position discrimination task in which the behavioral response purely relied on the target's allocentric location, independent of its egocentric position. We used two conditions of stimulus location: the compatible condition-allocentric left and egocentric left or allocentric right and egocentric right; the incompatible condition-allocentric left and egocentric right or allocentric right and egocentric left. We found that egocentric representation markedly influenced allocentric perception in three ways. First, in a given egocentric location, allocentric perception was significantly faster in the compatible condition than in the incompatible condition. Second, as the target became more eccentric in the visual field, the speed of allocentric perception gradually slowed down in the incompatible condition but remained unchanged in the compatible condition. Third, egocentric-allocentric incompatibility slowed allocentric perception more in the left egocentric side than the right egocentric side. These results cannot be explained by interhemispheric visuomotor transformation and stimulus-response compatibility theory. Our findings indicate that each hemisphere preferentially processes and integrates the contralateral egocentric and allocentric spatial information, and the right hemisphere receives more ipsilateral egocentric inputs than left hemisphere does.     

Common and specific neural correlates underlying the spatial congruency effect induced by the egocentric and allocentric reference frame

The spatial location of an object can be represented in two frames of reference: egocentric (relative to the observer's body or body parts) and allocentric (relative to another object independent of the observer). The object positions relative to the two frames can be either congruent (e.g., both left or both right) or incongruent (e.g., one left and one right). Most of the previous studies, however, did not discriminate between the two types of spatial conflicts. To investigate the common and specific neural mechanisms underlying the spatial congruency effect induced by the two reference frames, we adopted a 3 (type of task: allocentric, egocentric, and color) × 2 (spatial congruency: congruent vs. incongruent) within‐subject design in this fMRI study. The spatial congruency effect in the allocentric task was induced by the task‐irrelevant egocentric representations, and vice versa in the egocentric task. The nonspatial color task was introduced to control for the differences in bottom‐up stimuli between the congruent and incongruent conditions. Behaviorally, significant spatial congruency effect was revealed in both the egocentric and allocentric task. Neurally, the dorsal‐medial visuoparietal stream was commonly involved in the spatial congruency effect induced by the task‐irrelevant egocentric and allocentric representations. The right superior parietal cortex and the right precentral gyrus were specifically involved in the spatial congruency effect induced by the irrelevant egocentric and allocentric representations, respectively. Taken together, these results suggested that different subregions in the parieto‐frontal network played different functional roles in the spatial interaction between the egocentric and allocentric reference frame. Hum Brain Mapp 38:2112–2127, 2017. © 2017 Wiley Periodicals, Inc.     

The neural basis of ego- and allocentric reference frames in spatial navigation: evidence from spatio-temporal coupled current density reconstruction

Different strategies in spatial navigation during passages through computer-simulated tunnels were investigated by means of EEG source reconstruction. The tunnels consisted of straight and curved segments and provided only visual flow, but no landmark, information. At the end of each tunnel passage, subjects had to indicate their end position relative to the starting point of the tunnel. Even though the visual information was identical for all subjects, two different strategy groups were identified: one group using an egocentric and the other group an allocentric reference frame. The current density reconstruction revealed the use of one or the other reference frame to be associated with distinct cortical activation patterns during critical stages of the task. For both strategy groups, an occipito-temporal network was dominantly active during the initial, straight tunnel segment. With turns in the tunnel, however, the activation patterns started to diverge, reflecting translational and/or rotational changes in the underlying coordinate systems. Computation of an egocentric reference frame was associated with prevailing activity within a posterior parietal-premotor network, with additional activity in frontal areas. In contrast, computation of an allocentric reference frame was associated with dominant activity within an occipito-temporal network, confirming right-temporal structures to play a crucial role for an allocentric representation of space.     

Both egocentric and allocentric cues support spatial priming in visual search

The perception-action model proposes that vision for perception and vision for action are subserved by two separate cortical systems, the ventral and dorsal streams, respectively [Milner, A. D., & Goodale, M. A. (1995). The visual brain in action (1st ed.). Oxford: Oxford University Press; Milner, A. D., & Goodale, M. A. (2006). The visual brain in action (2nd ed.). Oxford: Oxford University Press Inc.]. The dorsal stream codes spatial information egocentrically, that is, relative to the observer. Egocentric representations are argued to be highly transient; therefore, it might be expected that egocentric information cannot be used for spatial memory tasks, even when the visual information only needs to be retained for a few seconds. Here, by applying a spatial priming paradigm to a visual search task, we investigated whether short-term spatial memory can use egocentric information. Spatial priming manifests itself in speeded detection times for a target when that target appears in the same location it previously appeared in. Target locations can be defined in either egocentric or allocentric (i.e. relative to other items in the display) frames of reference; however, it is unclear which of these are used in spatial priming, or if both are. Our results show that both allocentric and egocentric cues were used in spatial priming, and that egocentric cues were in fact more effective than allocentric cues for short-term priming. We conclude that egocentric information can persist for several seconds; a conclusion which is at odds with the assumption of the perception-action model that egocentric representations are highly transient.     

Spatial deficits and hemispheric asymmetries in the rat following unilateral and bilateral lesions of posterior parietal or medial agranular cortex

Studies of spatial behavior in both the human and non-human primate have generally focused on the role of the posterior parietal and prefrontal cortices and have indicated that destruction of these regions produce allocentric and egocentric deficits, respectively. The present study examined the role of the rodent analogs of these regions, the posterior parietal (PPC) and medial agranular (AGm) cortices, in egocentric and allocentric spatial processing, and whether spatial processing in rodents is organized in a hemispatial and/or lateralized manner as has been found in the primate. Eighty male rats receiving either a unilateral or bilateral lesion of AGm or PPC were examined on an egocentric (adjacent arm) or an allocentric (cheeseboard) maze task. The results indicated that PPC and AGm have dissociable spatial functions. Bilateral AGm destruction resulted in egocentric spatial deficits, and unilateral AGm operates demonstrated an intermediate deficit. In contrast, bilateral PPC operates demonstrated a severe deficit in allocentric processing. In addition, there were lateralized differences in the performance of unilateral PPC operates. While right PPC lesions resulted in a significant deficit on the allocentric task, no such deficit was seen in left PPC operates. In addition, neither unilateral AGm nor unilateral PPC operates demonstrated a hemispatial impairment on either the egocentric or allocentric tasks.     

Differential learning strategies in spatial and nonspatial versions of the Morris water maze in the C57BL/6J inbred mouse strain

We recently developed a new nonspatial version of the Morris water maze that requires the use of four visually distinct intra-maze patterns to efficiently locate a hidden platform. The nonspatial version was designed to match the spatial version on complexity of cue usage, and differs only on spatiality of cues, thereby allowing more meaningful comparisons between the two versions. Following a previous experiment that demonstrated nonspatial learning with the BXSB inbred mouse strain, C57 inbred mice were tested in this study. They received spatial and nonspatial training in a counter-balanced order so that Test Order and information transfer could be assessed. Subjects that received spatial training first had superior performance in both the spatial and the nonspatial tasks when compared to mice that received nonspatial training first. The mice that received spatial training first used extra-maze cues as a spatial strategy. However, during nonspatial testing they did not use the intra-maze cues to locate the platform; instead, the mice used an egocentric strategy of circling through the platform annulus. Subjects that received spatial testing first were superior on the nonspatial task to those subjects that received nonspatial training first. Moreover, subjects that received nonspatial testing first were unable to learn the spatial version. Overall, C57 mice can learn both the spatial and nonspatial versions of the Morris maze presented here; however, the nonspatial version is more difficult and is solved using an egocentric strategy.     

Detecting allocentric and egocentric navigation deficits in patients with schizophrenia and bipolar disorder using virtual reality

Present evidence suggests that the use of virtual reality has great advantages in evaluating visuospatial navigation and memory for the diagnosis of psychiatric or other neurological disorders. There are a few virtual reality studies on allocentric and egocentric memories in schizophrenia, but studies on both memories in bipolar disorder are lacking. The objective of this study was to compare the performance of allocentric and egocentric memories in patients with schizophrenia and bipolar disorder. For this resolve, an advanced virtual reality navigation task (VRNT) was presented to distinguish the navigational performances of these patients. Twenty subjects with schizophrenia and 20 bipolar disorder patients were compared with 20 healthy-matched controls on the newly developed VRNT consisting of a virtual neighbourhood (allocentric memory) and a virtual maze (egocentric memory). The results demonstrated that schizophrenia patients were significantly impaired on all allocentric, egocentric, visual, and verbal memory tasks compared with patients with bipolar disorder and normal subjects. Dissimilarly, the performance of patients with bipolar disorder was slightly lower than that of control subjects in all these abilities, but no significant differences were observed. It was concluded that allocentric and egocentric navigation deficits are detectable in patients with schizophrenia and bipolar disorder using VRNT, and this task along with RAVLT and ROCFT can be used as a valid clinical tool for distinguishing these patients from normal subjects.     

Frontal eye fields involved in shifting frame of reference within working memory for scenes

Working memory (WM) evoked by linguistic cues for allocentric spatial and egocentric spatial aspects of a visual scene was investigated by correlating fMRI BOLD signal (or "activation") with performance on a spatial-relations task. Subjects indicated the relative positions of a person or object (referenced by the personal pronouns "he/she/it") in a previously shown image relative to either themselves (egocentric reference frame) or shifted to a reference frame anchored in another person or object in the image (allocentric reference frame), e.g. "Was he in front of you/her?" Good performers had both shorter response time and more correct responses than poor performers in both tasks. These behavioural variables were entered into a principal component analysis. The first component reflected generalised performance level. We found that the frontal eye fields (FEF), bilaterally, had a higher BOLD response during recall involving allocentric compared to egocentric spatial reference frames, and that this difference was larger in good performers than in poor performers as measured by the first behavioural principal component. The frontal eye fields may be used when subjects move their internal gaze during shifting reference frames in representational space. Analysis of actual eye movements in three subjects revealed no difference between egocentric and allocentric recall tasks where visual stimuli were also absent. Thus, the FEF machinery for directing eye movements may also be involved in changing reference frames within WM.     

The double-H maze test, a novel, simple, water-escape memory task: acquisition, recall of recent and remote memory, and effects of systemic muscarinic or NMDA receptor blockade during training

To explore spatial cognition in rodents, research uses maze tasks, which differ in complexity, number of goals and pathways, behavioural flexibility, memory duration, but also in the experimenter's control over the strategy developed to reach a goal (e.g., allocentric vs. egocentric). This study aimed at validating a novel spatial memory test: the double-H maze test. The transparent device made of an alley with two opposite arms at each extremity and two in its centre is flooded. An escape platform is submerged in one arm. For experiments 1-3, rats were released in unpredictable sequences from one of both central arms to favour an allocentric approach of the task. Experiment 1 (3 trials/day over 6 days) demonstrated classical learning curves and evidence for recent and nondegraded remote memory performance. Experiment 2 (2 days, 3 trials/day) showed a dose-dependent alteration of task acquisition/consolidation by muscarinic or NMDA receptor blockade; these drug effects vanished with sustained training (experiment 3; 4 days, 3 trials/day). Experiment 4 oriented rats towards a procedural (egocentric) approach of the task. Memory was tested in a misleading probe trial. Most rats immediately switched from response learning-based to place learning-based behaviour, but only when their initial view on environmental cues markedly differed between training and probe trials. Because this simple task enables the formation of a relatively stable memory trace, it could be particularly adapted to study consolidation processes at a system level or/and the interplay between procedural and declarative-like memory systems.     

A role for the head-direction system in geometric learning

Several recent models of episodic memory have highlighted a potential contribution from the head-direction system; there is, however, surprisingly little known about the behavioural effects of selective lesions within the head-direction system. To address this issue, and determine what aspects of spatial memory are dependent on the head-direction system, rats with selective lateral mammillary body lesions were tested on tasks that required the use of specific spatial cues, including direction, visual allocentric, and geometric cues. Animals were first tested on a modified version of the T-maze alternation task that enabled the systematic removal of intramaze and visual allocentric cues. Rats were next tested on a geometric task that required the use of the shape of the environment to locate a hidden platform in the water-maze. The lesion rats were impaired on one stage of the T-maze alternation task and on the acquisition of the geometric task; these results are consistent with the head-direction system contributing to the processing of, and/or subsequent use, of visual allocentric and geometric cues. From the pattern of impairments it also appears that, with training, rats with lateral mammillary body lesions are able to recruit other navigational systems or that there is some degree of redundancy within the head-direction system.     

Cholinergic receptor blockade in prefrontal cortex and lesions of the nucleus basalis: implications for allocentric and egocentric spatial memory in rats

In this study we have examined the involvement of the prefrontal cortex (PFC) along with the Nucleus basalis magnocellularis (NBM) in two types of spatial navigation tasks. We evaluated the effects of excitotoxic (ibotenate-induced) lesions of the NBM in an allocentric and an egocentric task in the Morris water maze, using sham operations for a comparison. In both cases we also assessed the effects of local cholinergic receptor blockade in the PFC by infusing the muscarinic receptor antagonist scopolamine (4 or 20 microg). Anatomically, the results obtained showed that this lesion produced a profound loss of acetylcholinesterase (AChE) positive cells in the NBM, and a loss of AChE positive fibres in most of the neocortex, but hardly in the medial PFC. Behaviourally, such lesions led to a severe impairment in the allocentric task. Intraprefrontal infusions of scopolamine led to a short-lasting impairment in task performance when the high dose was used. In the second experiment, using the same surgical manipulations, we examined the performance in the egocentric task. Like in the allocentric task animals with NBM lesions were also impaired, but with continued training they acquired a level of performance similar to the sham-operated ones. This time, infusions of scopolamine in the medial PFC led to a severe disruption of performance in both groups of animals. We conclude that acetylcholine in the medial PFC is important for egocentric but not allocentric spatial memory, whereas the NBM is involved in the learning of both tasks, be it to a different degree.     

Dissociation of egocentric and allocentric coding of space in visual search after right middle cerebral artery stroke

Spatial representations rely on different frames of reference. Patients with unilateral neglect may behave as suffering from either egocentric or allocentric deficiency. The neural substrates representing these reference frames are still under discussion. Here we used a visual search paradigm to distinguish between egocentric and allocentric deficits in patients with right hemisphere cortical lesions. An attention demanding search task served to divide patients according to egocentric versus allocentric deficits. The results indicate that egocentric impairment was associated with damage in premotor cortex involving the frontal eye fields. Allocentric impairment on the other hand was linked to lesions in more ventral regions near the parahippocampal gyrus (PHG).