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.     

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.     

Navigation strategies in patients with vestibular loss tested in a virtual reality T-maze

Journal of Neurology - During navigation, humans mainly rely on egocentric and allocentric spatial strategies, two different frames of reference working together to build a coherent representation...     

A stable home‐base promotes allocentric memory representations of episodic‐like everyday spatial memory

A key issue in neurobiological studies of episodic‐like memory is the geometric frame of reference in which memory traces of experience are stored. Assumptions are sometimes made that specific protocols favour either allocentric (map‐like) or egocentric (body‐centred) representations. There are, however, grounds for suspecting substantial ambiguity about coding strategy, including the necessity to use both frames of reference occasionally, but tests of memory representation are not routinely conducted. Using rats trained to find and dig up food in sandwells at a particular place in an event arena (episodic‐like 'action‐where' encoding), we show that a protocol previously thought to foster allocentric encoding is ambiguous but more predisposed towards egocentric encoding. Two changes in training protocol were examined with a view to promoting preferential allocentric encoding—one in which multiple start locations were used within a session as well as between sessions; and another that deployed a stable home‐base to which the animals had to carry food reward. Only the stable home‐base protocol led to excellent choice performance which rigorous analyses revealed to be blocked by occluding extra‐arena cues when this was done after encoding but before recall. The implications of these findings for studies of episodic‐like memory are that the representational framework of memory at the start of a recall trial will likely include a path direction in the egocentric case but path destination in the allocentric protocol. This difference should be observable in single‐unit recording or calcium‐imaging studies of spatially‐tuned cells.     

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.     

Spatial memory and the monkey hippocampus: not all space is created equal

Studies of the role of the monkey hippocampus in spatial learning and memory, however few, have reliably produced inconsistent results. Whereas the role of the hippocampus in spatial learning and memory has been clearly established in rodents, studies in nonhuman primates have made a variety of claims that range from the involvement of the hippocampus in spatial memory only at relatively longer memory delays, to no role for the hippocampus in spatial memory at all. In contrast, we have shown that selective damage restricted to the hippocampus (CA regions) prevents the learning or use of allocentric, spatial relational representations of the environment in freely behaving adult monkeys tested in an open-field arena. In this commentary, we discuss a unifying framework that explains these apparently discrepant results regarding the role of the monkey hippocampus in spatial learning and memory. We describe clear and strict criteria to interpret the findings from previous studies and guide future investigations of spatial memory in monkeys. Specifically, we affirm that, as in the rodent, the primate hippocampus is critical for spatial relational learning and memory, and in a time-independent manner. We describe how claims to the contrary are the result of experimental designs that fail to recognize, and control for, egocentric (hippocampus-independent) and allocentric (hippocampus-dependent) spatial frames of reference. Finally, we conclude that the available data demonstrate unequivocally that the central role of the hippocampus in allocentric, spatial relational learning and memory is conserved among vertebrates, including nonhuman primates.     

Opposite visual field asymmetries for egocentric and allocentric spatial judgments

The purpose of the present study was to investigate the relation between visual hemifields and spatial frames of reference, according to the idea that multiple representations of 3D space exist. Results from two experiments clearly show that an upper visual hemifield advantage only arises when allocentric spatial judgments are required in order to perform a location task, whereas a lower visual hemifield advantage arises when egocentric spatial judgments are required. Such a double dissociation was interpreted as due to the activity of two separate neural pathways operating specific transformations of visual input for different functional outputs: scene recognition, mostly relying on allocentric frames of reference and subserved by the ventral, occipito-temporal pathway of the visual system, and goal directed actions, mostly relying on egocentric systems and subserved by the dorsal, occipito-parietal pathway of the visual system.     

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.     

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.     

Posterior parahippocampal gyrus lesions in the human impair egocentric learning in a virtual environment

Functional imaging studies have shown that the posterior parahippocampal gyrus (PHG) is involved in allocentric (world-centered) object and scene recognition. However, the putative role of the posterior PHG in egocentric (body-centered) spatial memory has received only limited systematic investigation. Thirty-one subjects with pharmacoresistant medial temporal lobe epilepsy (TLE) and temporal lobe removal were compared with 19 matched healthy control subjects on a virtual reality task affording the navigation in a virtual maze (egocentric memory). Lesions of the hippocampus and PHG of TLE subjects were determined by three-dimensional magnetic resonance imaging volumetric assessment. The results indicate that TLE subjects with right-sided posterior PHG lesions were impaired on virtual maze acquisition when compared with controls and TLE subjects with anterior PHG lesions. Larger posterior PHG lesions were significantly related to stronger impairments in virtual maze performance. Our results point to a role of the right-sided posterior PHG for the representation and storage of egocentric information. Moreover, access to both allocentric and egocentric streams of spatial information may enable the posterior PHG to construct a global and comprehensive representation of spatial environments.     

Egocentric and allocentric spatial reference frames in aging: A systematic review

Aging affects many aspects of everyday living, such as autonomy, security and quality of life. Among all, spatial memory and spatial navigation show a gradual but noticeable decline, as a result of both neurobiological changes and the general slowing down of cognitive functioning. We conducted a systematic review using the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines to identify studies that specifically investigated the role of allocentric and egocentric frames in healthy aging. Concerning spatial navigation, our results showed a preservation of egocentric strategies, along with specific impairments in the use of allocentric and switching abilities. Regarding spatial memory, instead, outcomes were more divergent and not frame-specific. With this perspective, spatial impairments were discussed considering the cognitive profile of mild cognitive impairment (MCI) and Alzheimer’s Disease (AD).     

Selective rotation of egocentric spatial representation following right putaminal hemorrhage

Although the role of frontoparietal cortex in spatial egocentric processing is well established, recent animal-lesion and human functional imaging studies have suggested that the neostriatum may also be a critical modulator in the processing of body-centred spatial orientation. We describe here a patient with right putamen-centred hemorrhage who exhibited a consistent counterclockwise rotation of approximately 90 degrees when drawing and writing from memory. A more detailed assessment with a series of representational clock tests demonstrated that the rotation was present only in tasks requiring the use of egocentric cues. In the absence of external cues the patient would adopt and maintain a stable but incorrectly-oriented egocentric representation of the imagined or recollected object. By contrast, performance could be rectified by presentation of correctly-oriented stimuli. These findings suggest that the putamen is part of a circuit underlying egocentric, as opposed to allocentric, representation of space in humans.     

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.     

Recognition memory for hand positions and spatial locations in patients with Huntington's disease: differential visuospatial memory impairment?

Allocentric and egocentric memory was investigated in patients with Huntington's disease (HD) and matched controls. Patients with HD and age- and education-matched healthy normal controls (NC) were administered two visuospatial recognition memory tasks, one assessing memory for hand positions (egocentric) and the other assessing memory for spatial locations (allocentric). HD patients showed normal primacy and recency effects, but their overall performance was impaired relative to controls on both tasks. Correlation analyses indicated that HD patients' performance on the Hand Position Memory task, but not the Spatial Location Memory task, was associated with global cognitive status (Mattis Dementia Rating Scale) and disease severity (Shoulson and Fahn Rating Scale), and HD patients' performances on the two tasks were not associated. Results provide preliminary support for the role of the caudate nucleus in both allocentric and egocentric spatial memory.     

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).     

Egocentric memory impaired and allocentric memory intact as assessed by virtual reality in subjects with unilateral parietal cortex lesions

Present evidence suggests that medial temporal cortices subserve allocentric representation and memory, whereas egocentric representation and memory mainly depends on inferior and superior parietal cortices. Virtual reality environments have a major advantage for the assessment of spatial navigation and memory formation, as computer-simulated first-person environments can simulate navigation in a large-scale space. However, virtual reality studies on allocentric memory in subjects with cortical lesions are rare, and studies on egocentric memory are lacking. Twenty-four subjects with unilateral parietal cortex lesions due to infarction or intracerebral haemorrhage (14 left-sided, 10 right-sided) were compared with 36 healthy matched control subjects on two virtual reality tasks affording to learn a virtual park (allocentric memory) and a virtual maze (egocentric memory). Subjects further received a comprehensive clinical and neuropsychological investigation, and MRI lesion assessment using T₁, T₂ and FLAIR sequences as well as 3D MRI volumetry at the time of the assessment. Results indicate that left- and right-sided lesioned subjects did not differ on task performance. Compared with control subjects, subjects with parietal cortex lesions were strongly impaired learning the virtual maze. On the other hand, performance of subjects with parietal cortex lesions on the virtual park was entirely normal. Volumes of the right-sided precuneus of lesioned subjects were significantly related to performance on the virtual maze, indicating better performance of subjects with larger volumes. It is concluded that parietal cortices support egocentric navigation and imagination during spatial learning in large-scale environments.     

Spatial deficits in an amnesic patient with hippocampal damage: questioning the multiple trace theory

Mediotemporal lobe structures are involved in both spatial processing and long-term memory. Patient M.R. suffers from amnesia, due to bilateral hippocampal lesion and temporoparietal atrophy following carbon monoxide poisoning. We compared his performance in immediate spatial memory tasks with the performance of ten healthy matched participants. Using an immediate reproduction of path, we observed a dissociation between his performance in three allocentric tasks and in five egocentric-updating tasks. His performance was always impaired on tasks requiring the use of an egocentric-updating representation but remained preserved on allocentric tasks. These results fit with the hypothesis that the hippocampus plays a role in spatial memory, but they also suggest that allocentric deficits previously observed in amnesia might actually reflect deficits in egocentric-updating processes. Furthermore, the co-occurrence of deficits in episodic long-term memory and short-term egocentric-updating representation without any short-term allocentric deficit suggests a new link between the mnemonic and navigational roles of the hippocampus. The Cognitive Map theory, the Multiple Trace theory, as well as further models linking spatial and nonspatial functions of the hippocampus are discussed.     

A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage

The spatial memory of a single patient (YR) was investigated. This patient, who had relatively selective bilateral hippocampal damage, showed the pattern of impaired recall but preserved item recognition on standardised memory tests that has been suggested by Aggleton and Shaw [Aggleton JP, Shaw C. Amnesia and recognition memory: a reanalysis of psychometric data. Neuropsychologia 1996;34:51-62] to be a consequence of Papez circuit lesions. YR was tested on three recall tests and one recognition test for visuospatial information. The initial recall test assessed visuospatial memory over very short unfilled delays and YR was not significantly impaired. This test was then modified to test recall of allocentric and egocentric spatial information separately after filled delays of between 5 and 60 s. YR was found to be more impaired at recalling allocentric than egocentric information after a 60 s interval with a tendency for the impairment to increase up to this delay. Recognition of allocentric spatial information was also assessed after delays of 5 and 60 s. YR was impaired after the 60 s delay. The results suggest that the human hippocampus has a greater involvement in allocentric than egocentric spatial memory, and that this most likely concerns the consolidation of allocentric information into long-term memory rather than the initial encoding of allocentric spatial information. The findings also suggest that YR's item recognition/free recall deficit pattern reflects a problem retrieving or storing certain kinds of associative information.     

Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment

Present evidence suggests that medial temporal cortices subserve allocentric representation and memory, whereas egocentric representation and memory also depends on parietal association cortices and the striatum. Virtual reality environments have a major advantage for the assessment of spatial navigation and memory formation, as computer-simulated first-person environments can simulate navigation in a large-scale space. Twenty-nine patients with amnestic MCI (aMCI) were compared with 29 healthy matched controls on two virtual reality tasks affording to learn a virtual park (allocentric memory) and a virtual maze (egocentric memory). Participants further received a neuropsychological investigation and MRI volumetry at the time of the assessment. Results indicate that aMCI patients had significantly reduced size of the hippocampus bilaterally and the right-sided precuneus and inferior parietal cortex. aMCI patients were severely impaired learning the virtual park and the virtual maze. Smaller volumes of the right-sided precuneus were related to worse performance on the virtual maze. Participants with striatal lacunar lesions committed more errors than participants without such lesions on the virtual maze but not on the virtual park. aMCI patients later converting to dementia (n = 15) had significantly smaller hippocampal size when compared with non-converters (n = 14). However, both groups did not differ on virtual reality task performance. Our study clearly demonstrates the feasibility of virtual reality technology to study spatial memory deficits of persons with aMCI. Future studies should try to design spatial virtual reality tasks being specific enough to predict conversion from MCI to dementia and conversion from normal to MCI.