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.     

l-DOPA changes ventral striatum recruitment during motor sequence learning in Parkinson's disease

Recent research indicates that longstanding temporal lobe epilepsy (TLE) is associated with extratemporal, i.e. parietal cortex damage. We investigated egocentric and allocentric memory by use of first-person large-scale virtual reality environments in patients with TLE. We expected that TLE patients with parietal cortex damage were impaired in the egocentric memory task. Twenty-two TLE patients with hippocampal sclerosis (HS) and 22 TLE patients without HS were compared with 42 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. When compared with controls, TLE patients with HS had significantly reduced size of the ipsilateral and contralateral somatosensory cortex (postcentral gyrus). When compared with controls or TLE patients without HS, TLE patients with HS were severely impaired learning the virtual maze. Considering all participants, smaller volumes of the left-sided postcentral gyrus were related to worse performance on the virtual maze. It is concluded that the paradigm of egocentric navigation and learning in first-person large-scale virtual environments may be a suitable tool to indicate significant extratemporal damage in individuals with TLE.     

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.     

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.     

Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia

Present evidence suggests that schizophrenia is associated with explicit memory deficits, whereas implicit memory seems to be largely preserved. Virtual reality studies on declarative allocentric memory in schizophrenia are rare, and studies on implicit egocentric memory in schizophrenia are lacking. However, virtual realities 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-five subjects with recent-onset schizophrenia were compared with 25 healthy matched control subjects on two virtual reality tasks affording the navigation and learning of a virtual park (allocentric memory) and a virtual maze (egocentric memory). Compared with control subjects, schizophrenia subjects were significantly impaired in learning the virtual park. However, schizophrenia subjects were as able as control subjects to learn the virtual maze. Stronger disorganized symptoms of schizophrenia subjects were significantly related to more errors on the virtual maze. It is concluded that egocentric spatial learning adds to the many other implicit cognitive skills being largely preserved in schizophrenia. Possibly, the more global neural network supporting egocentric spatial learning is less affected than the declarative hippocampal memory system in early stages of schizophrenia and may offer opportunities for compensation in the presence of focal deficits.     

As the world turns: short-term human spatial memory in egocentric and allocentric coordinates

We aimed to determine whether human subjects' reliance on different sources of spatial information encoded in different frames of reference (i.e., egocentric versus allocentric) affects their performance, decision time and memory capacity in a short-term spatial memory task performed in the real world. Subjects were asked to play the Memory game (a.k.a. the Concentration game) without an opponent, in four different conditions that controlled for the subjects' reliance on egocentric and/or allocentric frames of reference for the elaboration of a spatial representation of the image locations enabling maximal efficiency. We report experimental data from young adult men and women, and describe a mathematical model to estimate human short-term spatial memory capacity. We found that short-term spatial memory capacity was greatest when an egocentric spatial frame of reference enabled subjects to encode and remember the image locations. However, when egocentric information was not reliable, short-term spatial memory capacity was greater and decision time shorter when an allocentric representation of the image locations with respect to distant objects in the surrounding environment was available, as compared to when only a spatial representation encoding the relationships between the individual images, independent of the surrounding environment, was available. Our findings thus further demonstrate that changes in viewpoint produced by the movement of images placed in front of a stationary subject is not equivalent to the movement of the subject around stationary images. We discuss possible limitations of classical neuropsychological and virtual reality experiments of spatial memory, which typically restrict the sensory information normally available to human subjects in the real world.     

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.     

Risk factors for spatial memory impairment in patients with temporal lobe epilepsy

At present, the risk factors for world-centered (allocentric) navigation impairment in patients with temporal lobe epilepsy (TLE) are not known. There is some evidence on the importance of the right hippocampus but other clinical features have not been investigated yet. In this study, we used an experimental human equivalent to the Morris water maze to examine spatial navigation performance in patients with drug-refractory unilateral TLE. We included 47 left-hemisphere speech dominant patients (25 right sided; 22 left sided). The aim of our study was to identify clinical and demographic characteristics of TLE patients who performed poorly in allocentric spatial memory tests.Our results demonstrate that poor spatial navigation is significantly associated with younger age at epilepsy onset, longer disease duration, and lower intelligence level. Allocentric navigation in TLE patients was impaired irrespective of epilepsy lateralization. Good and poor navigators did not differ in their age, gender, or preoperative/postoperative status.This study provides evidence on risk factors that increase the likelihood of allocentric navigation impairment in TLE patients. The results indicate that not only temporal lobe dysfunction itself but also low general cognitive abilities may contribute to the navigation impairment.     

Altered white matter integrity in temporal lobe epilepsy: Association with cognitive and clinical profiles

Purpose: Diffusion tensor imaging (DTI) studies have reported substantial white matter abnormalities in patients with temporal lobe epilepsy (TLE). However, limited data exist regarding the extent of white matter tract abnormalities, cognitive effects of these abnormalities, and relationship to clinical factors. The current study examined these issues in subjects with chronic TLE. Methods: DTI data were obtained in 12 TLE subjects and 10 age‐matched healthy controls. Voxel‐wise statistical analysis of fractional anisotropy (FA) was carried out using tract‐based spatial statistics (TBSS). White matter integrity was correlated with cognitive performance and epilepsy‐related clinical parameters. Results: Subjects with TLE, as compared to healthy controls, demonstrated four clusters of reduced FA, in anterior temporal lobe, mesial temporal lobe, and cerebellum ipsilateral, as well as frontoparietal lobe contralateral to the side of seizure onset. Mean FA was positively correlated with delayed memory, in anterior temporal lobe; and immediate memory, in mesial temporal lobe. Lower FA values in the posterior region of corpus callosum were related to earlier age of seizure onset. Conclusion: TLE is associated with widespread disturbances in white matter tracts and these changes have important cognitive and clinical consequences.     

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.     

Perirhinal cortex involvement in allocentric spatial learning in the rat: Evidence from doubly marked tasks

It has recently been suggested that the different cortices of the medial temporal lobe support a mixture of object and spatial processing functions, challenging the anterior model that emphasized a strict functional differentiation between regions. However, for some structures, the perirhinal cortex (Prh) for example, a number of studies using lesion methods have shown a profound deficit exclusively in tasks involving object learning but not allocentric spatial learning. It may be that the learning paradigms used in previous studies have not been sensitive enough to detect a possible allocentric deficit in Prh‐lesioned animals. To examine whether Prh lesions critically affect allocentric spatial learning, experimental and control rats were trained in two doubly marked navigation tasks. In experiment 1, the use of either one of two different memory systems, allocentric versus egocentric, made it possible to locate the goal arm in a four‐arm radial maze. In experiment 2, rats had to choose between an allocentric versus a S‐R/habit strategy, both of which predicted the location of the goal arm. Results showed that both experimental and control animals learned both navigation tasks well, reaching the same level of performance at the end of training. However, a probe test performed 1 day after the learning ended revealed that Prh‐damaged animals learned both tasks predominantly using a non‐allocentric strategy. Specifically, in lesioned subjects the percentage of egocentric correct responses (experiment 1) and the percentage of habit‐based correct responses (experiment 2) was significantly higher than in the control rats. On the other hand, in both experiments, control rats in the probe test presented a significantly higher number of allocentric correct responses than the lesioned subjects. These results clearly suggest that Prh is normally needed for using allocentric strategies in order to solve a navigation problem. © 2017 Wiley Periodicals, Inc.     

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. Hum Brain Mapp, 2013. © 2012 Wiley Periodicals, Inc.     

Memory relationships between MRI volumes and resting PET metabolism of medial temporal lobe structures

Prior studies of temporal lobe epilepsy (TLE) patients showed that MRI volumes and resting PET scan measures of temporal lobe structures were related to memory. Weintrob and colleagues [Ann. Neurol. 2002;51:442-7] reported that PET glucose uptake in the left perirhinal cortex predicted verbal paired associate (PA) learning, whereas MRI volume of the left hippocampus did not. We investigated whether MRI volumes could account for memory functioning if both PET and volumes were from the same region in 18 TLE patients. Volumes and glucose uptake of the hippocampus and parahippocampal gyrus (PHG) were compared with WMS-III performance. Significant correlations were observed between hippocampal volumes and PA and Logical Memory (LM) Percent Retention, but not between memory and PHG volumes or any PET measures. Multiple regression revealed that hippocampal volumes, but not PHG volumes or PET, significantly predicted PA and LM retention scores. These findings suggest that hippocampal volumes provide unique information regarding memory.     

Disrupted allocentric but preserved egocentric spatial learning in transgenic mice with impaired glucocorticoid receptor function

Spatial and non-spatial learning of mice with an incorporated antisense RNA complementary to a fragment of cDNA coding for the glucocorticoid receptor (GR) were evaluated in allocentric and egocentric radial maze and water maze tasks, and in spontaneous object recognition and sensorimotor learning paradigms. Mice with impaired GR function did not acquire two maze paradigms based on allocentric spatial navigation, radial maze non-matching to position and water maze spatial discrimination learning. Comparison of performance in spaced and massed trials indicated that this may be due to a general inability to store information into allocentric reference memory or in retrieval processes. However, both groups of animals learned the rules of an egocentric radial maze task at similar rates and there was no difference in their ability to recognise objects once animals had equal opportunity to explore the sample objects. Sensorimotor performance was impaired in transgenic animals, but it is suggested that this is due to non-specific factors rather than to disrupted sensorimotor learning per se. These results are consistent with a disruption of hippocampal function. Histological examination of the hippocampus revealed no obvious structural abnormalities in transgenic animals. Therefore, the data suggest that functional underactivity of GRs at the level of the hippocampus induces a deficit in allocentric navigation while sparing egocentric navigation and object recognition.     

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.     

Impaired associative memory in temporal lobe epilepsy subjects after lesions of hippocampus, parahippocampal gyrus, and amygdala

There has been growing interest in the differential role of medial temporal lobe structures in learning and memory. The goal of the present study was to clarify how lesions of hippocampus, parahippocampal gyrus, and amygdala interfere with associative learning and memory. Thirty subjects with pharmacoresistant medial temporal lobe epilepsy (TLE) and temporal lobe removal were compared with 30 matched healthy control subjects. A set of neuropsychological test measures and an associative learning task requiring the learning and recall of objects and faces were administered. The lesions of hippocampus, parahippocampal gyrus, amygdala, and fusiform gyrus of TLE subjects were determined by three-dimensional magnetic resonance imaging (3-D MRI) volumetric assessment. The results indicate that TLE subjects with combined large hippocampal lesions, large parahippocampal gyrus (i.e., perirhinal/entorhinal) lesions, and large amygdala lesions learned and recalled the associative task significantly worse than control subjects or subjects with small lesions of the hippocampus, parahippocampal gyrus, and amygdala. Regression analysis revealed that larger lesions of the parahippocampal gyrus (i.e., perirhinal/entorhinal cortices) were significantly related to increasing deficits on the task, and that hippocampal and amygdala lesion size did not significantly improve the prediction. Our results suggest that perirhinal and entorhinal cortices may contribute predominantly to the associative learning and recall of objects and faces.     

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.     

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.     

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).