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.     

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.     

Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition

Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.     

Allocentric and egocentric spatial impairments in a case of topographical disorientation

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

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.     

Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans?

The claim that recognition memory is spared relative to recall after focal hippocampal damage has been disputed in the literature. We examined this claim by investigating object and object-location recall and recognition memory in a patient, YR, who has adult-onset selective hippocampal damage. Our aim was to identify the conditions under which recognition was spared relative to recall in this patient. She showed unimpaired forced-choice object recognition but clearly impaired recall, even when her control subjects found the object recognition task to be numerically harder than the object recall task. However, on two other recognition tests, YR's performance was not relatively spared. First, she was clearly impaired at an equivalently difficult yes/no object recognition task, but only when targets and foils were very similar. Second, YR was clearly impaired at forced-choice recognition of object-location associations. This impairment was also unrelated to difficulty because this task was no more difficult than the forced-choice object recognition task for control subjects. The clear impairment of yes/no, but not of forced-choice, object recognition after focal hippocampal damage, when targets and foils are very similar, is predicted by the neural network-based Complementary Learning Systems model of recognition. This model postulates that recognition is mediated by hippocampally dependent recollection and cortically dependent familiarity; thus hippocampal damage should not impair item familiarity. The model postulates that familiarity is ineffective when very similar targets and foils are shown one at a time and subjects have to identify which items are old (yes/no recognition). In contrast, familiarity is effective in discriminating which of similar targets and foils, seen together, is old (forced-choice recognition). Independent evidence from the remember/know procedure also indicates that YR's familiarity is normal. The Complementary Learning Systems model can also accommodate the clear impairment of forced-choice object-location recognition memory if it incorporates the view that the most complete convergence of spatial and object information, represented in different cortical regions, occurs in the hippocampus.     

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.     

Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition

In this study, we have examined visual recognition memory in a patient, YR, with discrete hippocampal damage who has shown normal or nearly normal item recognition over a large number of tests. We directly compared her performance as measured using a visual paired comparison task (VPC) with her performance on delayed matching to sample (DMS) tasks. We also investigated the effect of retention interval between familiarisation and test. YR shows good visual recognition with the DMS task up to 10 s after the familiarisation period, but only shows recognition with the VPC task for the shortest retention interval (0 s). Our results are consistent with the view that hippocampal damage disrupts recollection and recall, but not item familiarity memory.     

Perceptual and mnemonic matching-to-sample in humans: contributions of the hippocampus, perirhinal and other medial temporal lobe cortices

Two questions were addressed by the present study. The first was whether the previously reported item recognition deficit which is shown by amnesic patients may be due to a perceptual rather than a memory deficit. To address this question a group of amnesic patients were tested on a 14-choice forced-choice visual item recognition test which included a "simultaneous" condition in which the sample remained visible during the matching decision and a zero second delay. Eacott, Gaffan and Murray (1994) have reported an impairment in simultaneous matching-to-sample following perirhinal damage in monkeys. In our amnesic patients, a deficit was found only after filled delays of 10 seconds or longer and this was also the case for a subgroup of patients whose damage included the perirhinal cortex. The second question, which arose from the model of Aggleton and Brown (1999), was whether performance on the DMS task would remain intact following selective damage to the hippocampus. We tested a patient with bilateral damage to the hippocampus on the 14-choice DMS task and found that her performance was not significantly impaired at delays of up to 30 seconds.     

Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat

The present study provides evidence that lesions of the fornix (FNX) and of the perirhinal/postrhinal cortex (PPRH), which both disconnect the hippocampus from other brain regions, can lead to distinct patterns of behavioural impairments on tests of spatial memory and spontaneous object recognition. For example, whereas FNX lesions impaired allocentric spatial delayed alternation in a T-maze but generally spared a test of spontaneous object recognition, PPRH lesions produced the opposite pattern of results. Indeed, on the T-maze task PPRH animals significantly outperformed controls when the retention delay was increased to 60 s. In addition, some evidence was found that contributions from both the fornix and perirhinal/postrhinal cortex may be required when object and spatial information must be integrated. In an object-in-place test, for example, PPRH animals failed according to two measures, and FNX animals failed according to one measure, to discriminate objects that had remained in fixed locations from those that had exchanged locations with other objects. Neither lesion, however, affected performance of a visuospatial conditional task, a Pavlovian autoshaping task, or a one-pair pattern discrimination task. It is suggested that the perirhinal/postrhinal cortex, rather than being specialised for a particular type of associative learning, is important for processing complex visual stimuli.     

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.     

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.     

Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching.

A virtual reality environment was used to test memory performance for simulated "real-world" spatial and episodic information in a 22-year-old male, Jon, who has selective bilateral hippocampal pathology caused by perinatal anoxia. He was allowed to explore a large-scale virtual reality town and was then tested on his memory for spatial layout and for episodes experienced. Topographical memory was tested by assessing his ability to navigate, recognize previously visited locations, and draw maps of the town. Episodic memory was assessed by testing the retrieval of simulated events which consisted of collecting objects from characters while following a route through the virtual town. Memory for the identity of objects, as well as for where they were collected, from whom, and in what order, was also tested. While the first task tapped simple recognition memory, the latter three tested memory for context. Jon was impaired on all topographical tasks and on his recall of the context-dependent questions. However, his recognition of objects from the virtual town, and of "topographical" scenes (as evaluated by standard neuropsychological tests), was not impaired. These findings are consistent with the view that the hippocampus is involved in navigation, recall of long term allocentric spatial information and context-dependent episodic memory, but not visual pattern matching.     

Trends in comorbid sickle cell disease among stroke patients

BackgroundVisuospatial skills including spatial navigation are known to be impaired in Huntington's disease. Spatial navigation comprises two navigational frameworks, allocentric and egocentric. Several studies have associated the allocentric navigation with the hippocampus and the egocentric navigation with the striatum. The striatum is predominantly impaired from the early stages of Huntington's disease.ObjectiveTo find whether spatial navigation impairment is present in the early stages of Huntington's disease and to test the hypothesis that the egocentric navigation is predominantly affected compared to the allocentric navigation.MethodsIn nineteen patients with Huntington's disease the egocentric and the allocentric navigation skills were tested using the Blue Velvet Arena, a human analog of Morris Water Maze, and compared to nineteen age and gender-matched healthy controls. Cognitive functions, with emphasis on the executive functions, were also assessed.ResultsThe spatial navigation skills deteriorated with the increasing motor impairment in Huntington's disease. These changes only became apparent in patients with moderate functional impairment. No difference between the egocentric and the allocentric skills was seen.DiscussionSpatial navigation deficit is not an early marker of the cognitive dysfunction in Huntington's disease. We speculate that the striatal circuitry that is known to degenerate early in the course of Huntington's disease is not directly associated with the spatial navigation.     

Binding of visual and spatial short-term memory in Williams syndrome and moderate learning disability

A main aim of this study was to test the claim that individuals with Williams syndrome have selectively impaired memory for spatial as opposed to visual information. The performance of 16 individuals with Williams syndrome (six males, 10 females; mean age 18y 7mo [SD 7y 6mo], range 9y 1mo-30y 7mo) on tests of short-term memory for item and location information was compared with that shown by individuals with moderate learning difficulties (12 males, four females; mean age 10y 3mo [SD 1y], range 8y 6mo-11y 7mo) and typically developing children (six males, 10 females; mean age 6y 8mo [SD 7mo], range 5y 10mo-7y 9mo) of an equivalent level of visuospatial ability. A second aim was to determine whether individuals had impaired ability to 'bind' visual spatial information when required to recall 'item in location' information. In contrast to previous findings, there was no evidence that individuals with Williams syndrome were more impaired in the spatial than the visual memory condition. However, individuals with both Williams syndrome and moderate learning difficulties showed impaired memory for item in location information, suggesting that problems of binding may be generally associated with learning disability.     

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.     

Integration of cognitive allocentric information in visuospatial short-term memory through the hippocampus

Visuospatial short-term memory relies on a widely distributed neocortical network: some areas support the encoding process of the visually acquired spatial information, whereas other ares are more involved in the active maintenance of the encoded information. Recently, in a pointing to remembered targets task, it has been shown in healthy subjects that, for memory delays of 5 s, spatial errors are affected also by cognitive allocentric information, i.e., covert spatial information derived from a pure mental representation. We tested the effect of a lesion of the hippocampus on the accuracy of pointing movements toward remembered targets, with memory delays falling in the 0.5-30 s range. The spatial distributions of the two target sets we used (line and left-right) allowed the exploitation of cognitive allocentric spatial information: both sets were in the frontal plane, the line one being composed by eleven points distributed uniformly along a virtual line tilted 45 degrees away from the vertical, whereas the left-right set was composed by two workspaces symmetrically distributed at the extremes of a horizontal virtual line. We have found a significant difference between the performance of three hippocampal amnesic subjects and a group of normal controls for delays equal to or longer than 15 s, the difference being along the allocentric axis, i.e., the direction of the virtual line defined by the target set. On this basis we suggest that the hippocampal formation may enhance the spatial information processed within short-term memory with cognitive allocentric information. The association that may be operated through the neocortical-hippocampal loop of the newly acquired spatial information with well established spatial cognitive items could affect the precision of the short-term memory storage for memory delays exceeding about 15 s and might be the result of a modulation of the span of the spatial memory buffer along context-specific directions.     

Rhinal and dorsolateral prefrontal cortex lesions produce selective impairments in object and spatial learning and memory in canines

To examine the effects of rhinal and dorsolateral prefrontal cortex lesions on object and spatial recognition memory in canines, we used a protocol in which both an object (delayed nonmatching to sample, or DNMS) and a spatial (delayed nonmatching to position or DNMP) recognition task were administered daily. The tasks used similar procedures such that only the type of stimulus information to be remembered differed. Rhinal cortex (RC) lesions produced a selective deficit on the DNMS task, both in retention of the task rules at short delays and in object recognition memory. By contrast, performance on the DNMP task remained intact at both short and long delay intervals in RC animals. Subjects who received dorsolateral prefrontal cortex (dlPFC) lesions were impaired on a spatial task at a short, 5-second delay, suggesting disrupted retention of the general task rules; however, this impairment was transient, and long-term spatial memory performance was unaffected in dlPFC subjects. The present results provide support for the involvement of the RC in object, but not visuospatial, processing and recognition memory, whereas the dlPFC appears to mediate retention of a nonmatching rule. These findings support theories of functional specialization within the medial temporal lobe and frontal cortex and suggest that rhinal and dorsolateral prefrontal cortices in canines are functionally similar to analogous regions in other mammals.     

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.