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.     

Topographical disorientation in aging. Familiarity with the environment does matter

Topographical disorientation (TD) refers to navigational impairment as an effect of aging or brain damage. Decreases in navigational performance with aging are more due to deficits in the ability to mentally represent space in an object-centered (allocentric) than in a self-centered (egocentric) format. Familiarity/remoteness of spatial memory traces can represent a protective factor for TD in aging. Conversely, using newly learned information for assessment may lead to overestimating TD severity as it combines two contributing factors: heading (allocentric) disorientation and anterograde agnosia. A supplementary evaluation of TD with aging according to ecological spatial tasks is recommended. The core tasks should focus on landmark positioning, both on a blind map (allocentric) and along a route (egocentric) of the hometown so as to disentangle spatial memory for familiar/remote information from decline due to recent encoding of information.     

Impaired allocentric spatial memory underlying topographical disorientation

The cognitive processes supporting spatial navigation are considered in the context of a patient (CF) with possible very early Alzheimer's disease who presents with topographical disorientation. Her verbal memory and her recognition memory for unknown buildings, landmarks and outdoor scenes was intact, although she showed an impairment in face processing. By contrast, her navigational ability, quantitatively assessed within a small virtual reality (VR) town, was significantly impaired. Interestingly, she showed a selective impairment in a VR object-location memory test whenever her viewpoint was shifted between presentation and test, but not when tested from the same viewpoint. We suggest that a specific impairment in locating objects relative to the environment rather than relative to the perceived viewpoint (i.e. allocentric rather than egocentric spatial memory) underlies her topographical disorientation. We discuss the likely neural bases of this deficit in the light of related studies in humans and animals, focusing on the hippocampus and related areas. The specificity of our test indicates a new way of assessing topographical disorientation, with possible application to the assessment of progressive dementias such as Alzheimer's disease.     

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.     

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.     

Transcranial Direct Current Stimulation Accelerates Allocentric Target Detection

BackgroundPrevious research on hemispatial neglect has provided evidence for dissociable mechanisms for egocentric and allocentric processing. Although a few studies have examined whether tDCS to posterior parietal cortex can be beneficial for attentional processing in neurologically intact individuals, none have examined the potential effect of tDCS on allocentric and/or egocentric processing.Objective/hypothesisOur objective was to examine whether transcranial direct current stimulation (tDCS), a noninvasive brain stimulation technique that can increase (anodal) or decrease (cathodal) cortical activity, can affect visuospatial processing in an allocentric and/or egocentric frame of reference.MethodsWe tested healthy individuals on a target detection task in which the target – a circle with a gap – was either to the right or left of the viewer (egocentric), or contained a gap on the right or left side of the circle (allocentric). Individuals performed the task before, during, and after tDCS to the posterior parietal cortex in one of three stimulation conditions – right anodal/left cathodal, right cathodal/left anodal, and sham.ResultsWe found an allocentric hemispatial effect both during and after tDCS, such that right anodal/left cathodal tDCS resulted in faster reaction times for detecting stimuli with left-sided gaps compared to right-sided gaps.ConclusionsOur study suggests that right anodal/left cathodal tDCS has a facilitatory effect on allocentric visuospatial processing, and might be useful as a therapeutic technique for individuals suffering from allocentric neglect.     

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 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.     

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.     

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).     

Egocentric disorientation following bilateral parietal lobe damage

Aguirre and D'Esposito (1999) suggested a taxonomy and theoretical framework for understanding topographical disorders. One of the problems they described involved egocentric disorientation, in which deficits are not strictly confined to the topographical sphere but are seen on a wide variety of visuo-spatial paradigms. Here, we report a neuropsychological investigation of MU, a person with egocentric disorientation. To test the usefulness of Aguirre and D'Esposito's framework, we administered tests which were predicted to be easy or difficult for people with egocentric disorientation to show that MU was impaired on tasks sensitive to egocentric disorientation and that he showed adequate performance on tests sensitive to other types of topographical representation. Thus MU showed normal performance on a test of recognition of famous landmarks and he could identify photographs of personally familiar places in his home town, yet he could not say how to get from a recognised building to another place in his environment. His performance fulfils the criteria for egocentric disorientation and fits the predictions derived from Aguirre and D'Esposito's views.     

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.     

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.     

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.     

Allocentric neglect strongly associated with egocentric neglect

Following brain injury, many patients experience egocentric spatial neglect, where they fail to respond to stimuli on the contralesional side of their body. On the other hand, allocentric, object-based neglect refers to the symptom of ignoring the contralesional side of objects, regardless of the objects' egocentric position. There is an established tradition for considering these two phenomena as both behaviorally and anatomically dissociable. However, several studies and some theoretical work have suggested that these rather reflect two aspects of a unitary underlying disorder. Furthermore, in a recent large study Yue et al. [Archives of Physical Medicine and Rehabilitation 93 (2012) 156] reported that acute allocentric neglect is only observed in cases where substantial egocentric neglect is also present. In a new sample of right hemisphere stroke patients, we attempted to control for potential confounds by using a novel continuous measure for allocentric neglect (in addition to a recently developed continuous measure for egocentric neglect). Our findings suggest a strong association between egocentric and allocentric neglect. Consistent with the work of Yue et al. (2012), we found allocentric behavioral deficits only in conjunction with egocentric deficits as well as a large corresponding overlap for the anatomical regions associated with egocentric and with allocentric neglect. We discuss how different anatomical and behavioral findings can be explained in a unified physiologically plausible framework, whereby allocentric and egocentric effects interact.     

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.     

Pure topographical disorientation in a patient with right occipito-temporal lesion

We describe a patient who presented with a pure topographical disorientation after a stroke involving the right mesial occipito-temporal cortex. He could not point to external unseen landmarks or draw a map of his city, while he could recognize landmarks, and judge the distance, and describe the route between pairs of landmarks of the same city. He underwent standardized cognitive tests, and 6 tasks were used to assess a topographical orientation route-survey. This study provides evidence that topographical disorientation can be subdivided into very specific components. The results suggest that one of these components might refer to the processing of an allocentric map separable from the representation of route knowledge.     

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.     

Pure agraphia with topographical disorientation caused by right hemisphere lesion

A 69-year-old, right-handed, Japanese male patient presented with pure agraphia with topographical disorientation after hemorrhage in the right parietal lobe. Upon developing cerebral hemorrhage, he was referred to our hospital for close examination of agraphia. There was no paresis or clumsiness in his extremities. His speech was fluent and well-articulated. Neither aphasia nor reading impairments was found, although there was a clear writing impairment with effort and hesitation. His writing of both kanji and kana letters contained additional, absent or deformed strokes or parts. No hemianopia, prosopagnosia, constructional disturbances and dressing apraxia were found. He could recognize familiar buildings or landscapes, but often lost his way around well-known areas. MR images revealed subcortical lesions of precuneus, superior and inferior parietal lobules in the right hemisphere, around the posterior horn of the lateral ventricle. He revealed pure agraphia and topographical disorientation after the right brain haemorrhage, without dementia or personality change. These findings indicate that the right parietal lobe participates in the kinesthetic movements of writing. Some authers have been documented cases of aphasic agraphia or alexia with agraphia caused by right hemisphere damage in dextrals, but pure agraphia caused by the lesion in the right hemisphere is very rare.