Memory for visuospatial location following selective hippocampal sclerosis: the use of different coordinate systems

This study addressed the role of the medial temporal lobe regions and, more specifically, the contribution of the human hippocampus in memory for body-centered (egocentric) and environment-centered (allocentric) spatial location. Twenty-one patients with unilateral atrophy of the hippocampus secondary to long-standing epilepsy (left, n = 7; right, n = 14) and 15 normal control participants underwent 3 tasks measuring recall of egocentric or allocentric spatial location. Patients with left hippocampal sclerosis were consistently impaired in the allocentric conditions of all 3 tasks but not in the egocentric conditions. Patients with right hippocampal sclerosis were impaired to a lesser extent and in only 2 of the 3 tasks. It was concluded that hippocampal structures are crucial for allocentric, but not egocentric, spatial memory.     

Lateralization of the startle reflex circuit in humans: an examination with monaural probes following unilateral temporal lobe resection

Startle reflex (SR) modulation elicited by monaural probes during affective picture viewing was investigated in patients following left temporal lobectomy (LTL; n = 8) and right temporal lobectomy (RTL; n = 10) and in controls (n = 18). All patients had undergone anteromedial temporal lobe (ATL) resection. LTL participants exhibited attenuated overall SR magnitude. Affective SR modulation in controls was significant for left ear probes, at both eyes, but not for right ear probes. RTL but not LTL participants displayed significant startle attenuation during pleasant picture viewing. Results suggest that monaural startle probes primarily activate structures in the ipsilateral ATL and that the ATLs are interconnected, with the left ATL more critical in perceiving arousing properties of affective stimuli, necessary for affective SR modulation.     

Restriction of early exploratory forays effects specific aspects of spatial processing in weanling hamsters

Normally reared hamsters, but not hamsters reared on a liquid diet, demonstrated spatial memory for the location of odor cues in an allocentric task (Experiment 1). In Experiment 2, an egocentric task, liquid-reared hamsters detected a change in the spatial location of odor cues. In Experiment 3 liquidreared hamsters detected a change in the spatial location of two visual cues under allocentric task conditions. Female hamsters on a liquid diet retrieved their pups more often than dams on solid food, resulting in reduced exploratory opportunities for their pups during the period when olfaction mediates behavior. Hamsters in Experiment 4 experienced a direct restriction of early forays. The restricted-rearing group failed to detect a change in the spatial location of odor cues in an allocentric task. These findings suggest that restriction of early exploratory experience during a narrow period of development results in specific spatial processing deficits.     

Temporal dynamics of object location processing in allocentric reference frame

The spatial location of objects is processed in egocentric and allocentric reference frames, the early temporal dynamics of which have remained relatively unexplored. Previous experiments focused on ERP components related only to egocentric navigation. Thus, we designed a virtual reality experiment to see whether allocentric reference frame‐related ERP modulations can also be registered. Participants collected reward objects at the end of the west and east alleys of a cross maze, and their ERPs to the feedback objects were measured. Participants made turn choices from either the south or the north alley randomly in each trial. In this way, we were able to discern place and response coding of object location. Behavioral results indicated a strong preference for using the allocentric reference frame and a preference for choosing the rewarded place in the next trial, suggesting that participants developed probabilistic expectations between places and rewards. We also found that the amplitude of the P1 was sensitive to the allocentric place of the reward object, independent of its value. We did not find evidence for egocentric response learning. These results show that early ERPs are sensitive to the location of objects during navigation in an allocentric reference frame.     

Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory

Despite the connections of the retrosplenial cortex strongly suggesting a role in spatial memory, the lesion data to date have been equivocal. Whether subjects are impaired after retrosplenial lesions seems to depend on whether the lesions were aspirative or excitotoxic, with the latter failing to produce an impairment. A shortcoming of previous excitotoxic lesion studies is that they spared the most caudal part of the retrosplenial cortex. The present study thus used rats with extensive neurotoxic lesions of the retrosplenial cortex that encompassed the entire rostrocaudal extent of this region. These rats were consistently impaired on several tests that tax allocentric memory. In contrast, they were unimpaired on an egocentric discrimination task. Although the lesions did not appear to affect object recognition, clear deficits were found for an object-in-place discrimination. The present study not only demonstrates a role for the retrosplenial cortex in allocentric spatial memory, but also explains why previous excitotoxic lesions have failed to detect any deficits.     

Judging hand laterality from my or your point of view: Interactions between motor imagery and visual perspective

Motor imagery tasks (hand laterality judgment) are usually performed with respect to a self-body (egocentric) representation, but manipulations of stimulus features (hand orientation) can induce a shift to other's body (allocentric) reference frame. Visual perspective taking tasks are also performed in self-body perspective but a shift to an allocentric frame can be triggered by manipulations of context features (e.g., another person present in the to-be-judged scene). Combining hand laterality task and visual perspective taking, we demonstrated that both stimulus and context features can modulate motor imagery performance. In Experiment 1, participants judged laterality of a hand embedded in a human or non-human silhouette. Results showed that observing a human silhouette interfered with judgments on “egocentric hand stimuli” (right hand, fingers up). In Experiment 2, participants were explicitly required to judge laterality of a hand embedded in a human silhouette from their own (egocentric group) or from the silhouette's perspective (allocentric group). Consistent with previous results, the egocentric group was significantly faster than the allocentric group in judging fingers-up right hand stimuli. These findings showed that concurrent activation of egocentric and allocentric frames during mental transformation of body parts impairs participants’ performance due to a conflict between motor and visual mechanisms.     

A body-centred frame of reference drives spatial priming in visual search

Spatial priming in visual search is a well-documented phenomenon. If the target of a visual search is presented at the same location in subsequent trials, the time taken to find the target at this repeated target location is significantly reduced. Previous studies did not determine which spatial reference frame is used to code the location. At least two reference frames can be distinguished: an observer-related frame of reference (egocentric) or a scene-based frame of reference (allocentric). While past studies suggest that an allocentric reference frame is more effective, we found that an egocentric reference frame is at least as effective as an allocentric one (Ball et al. Neuropsychologia 47(6):1585–1591, 2009). Our previous study did not identify which specific egocentric reference frame was used for the priming: participants could have used a retinotopic or a body-centred frame of reference. Here, we disentangled the retinotopic and body-centred reference frames. In the retinotopic condition, the position of the target stimulus, when repeated, changed with the fixation position, whereas in the body-centred condition, the position of the target stimulus remained the same relative to the display, and thus to the body-midline, but was different relative to the fixation position. We used a conjunction search task to assess the generality of our previous findings. We found that participants relied on body-centred information and not retinotopic cues. Thus, we provide further evidence that egocentric information, and specifically body-centred information, can persist for several seconds, and that these effects are not specific to either a feature or a conjunction search paradigm.     

Frames of reference and categorical and coordinate spatial relations: a hierarchical organisation

This research is about the role of categorical and coordinate spatial relations and allocentric and egocentric frames of reference in processing spatial information. To this end, we asked whether spatial information is firstly encoded with respect to a frame of reference or with respect to categorical/coordinate spatial relations. Participants had to judge whether two vertical bars appeared on the same side (categorical) or at the same distance (coordinate) with respect to the centre of a horizontal bar (allocentric) or with respect to their body midline (egocentric). The key manipulation was the timing of the instructions: one instruction (reference frame or spatial relation) was given before stimulus presentation, the other one after. If spatial processing requires egocentric/allocentric encoding before coordinate/categorical encoding, then spatial judgements should be facilitated when the frame of reference is specified in advance. In contrast, if categorical and coordinate dimensions are primary, then a facilitation should appear when the spatial relation is specified in advance. Results showed that participants were more accurate and faster when the reference frame rather than the type of spatial relation was provided before stimulus presentation. Furthermore, a selective facilitation was found for coordinate and categorical judgements after egocentric and allocentric cues, respectively. These results suggest a hierarchical structure of spatial information processing where reference frames play a primary role and selectively interact with subsequent processing of spatial relations.     

Allocentric spatial memory activation of the hippocampal formation measured with fMRI

Hippocampal activation was investigated, comparing allocentric and egocentric spatial memory. Healthy participants were immersed in a virtual reality circular arena, with pattern-rendered walls. In a viewpoint-independent task, they moved toward a pole, which was then removed. They were relocated to another position and had to move to the prior location of the pole. For viewpoint-dependent memory, the participants were not moved to a new starting point, but the patterns were rotated to prevent them from indicating the final position. Hippocampal and parahippocampal activation were found in the viewpoint-independent memory encoding phase. Viewpoint-dependent memory did not result in such activation. These results suggest differential activation of the hippocampal formation during allocentric encoding, in partial support of the spatial mapping hypothesis as applied to humans.     

Prefrontal serotonin depletion impairs egocentric, but not allocentric working memory in rats

Working memory is a cognitive ability chiefly organized by the prefrontal cortex. Working memory tests may be resolved based on allocentric or egocentric spatial strategies. Serotonergic neurotransmission is closely involved in working memory, but its role in spatial strategies for working memory performance is unknown. To address this issue, prefrontal serotonin depletion was induced to adult male rats, and three days after the behavioral expression of both allocentric and egocentric strategies were evaluated in the "Y" maze and in a crossed-arm maze, respectively. Serotonin depletion caused no effects on allocentric-related behavioral performance, but lesioned rats performed deficiently when the egocentric working memory was evaluated. These results suggest that serotonin may be more closely related with the organization of working memory that uses own movement-guided responses than with that involving the use of external visuospatial signals. Further neurochemical studies are needed to elucidate possible interactions between serotonergic activity and other neurotransmitter systems in the organization of working memory-related allocentric and egocentric strategies.     

Cognitive allocentric representations of visual space shape pointing errors

Subjects reached in three-dimensional space to a set of remembered targets whose position was varied randomly from trial to trial, but always fell along a "virtual" line (line condition). Targets were presented briefly, one-by-one and in an empty visual field. After a short delay, subjects were required to point to the remembered target location. Under these conditions, the target was presented in the complete absence of allocentric visual cues as to its position in space. However, because the subjects were informed prior to the experiment that all targets would fall on a straight line, they could conceivably imagine each point target as belonging to a single rigid object with a particular geometry and orientation in space, although this virtual object was never explicitly shown to the subjects. We compared the responses to repeated measurements of each target with those measured for targets presented in a directionally neutral configuration (sphere condition), and used the variable errors to infer the putative reference frames underlying the corresponding sensorimotor transformation. Performance in the different tasks was compared under two different lighting conditions (dim light or total darkness) and two memory delays (0.5 or 5 s). The pattern of variable errors differed significantly between the sphere condition and the line condition. In the former case, the errors were always accounted for by egocentric reference frames. By contrast the errors in the line condition revealed both egocentric and allocentric components, consistent with the hypothesis that target information can be defined concurrently in both egocentric and allocentric frames of reference, resulting in two independent coexisting representations. Electronic Publication     

Frames of reference during implicit and explicit learning

There is a significant overlap between the processes and neural substrates of spatial cognition and those subserving memory and learning. However, for procedural learning, which often is spatial in nature, we do not know how different forms of spatial knowledge, such as egocentric and allocentric frames of reference, are utilized nor whether these frames are differentially engaged during implicit and explicit processes. To address this issue, we trained human subjects on a movement sequence presented on a bi-dimensional (2D) geometric frame. We then systematically manipulated the geometric frame (allocentric) or the sequence of movements (egocentric) or both, and retested the subjects on their ability to transfer the sequence knowledge they had acquired in training and also determined whether the subjects had learned the sequence implicitly or explicitly. None of the subjects (implicit or explicit) showed evidence of transfer when both frames of reference were changed which suggests that spatial information is essential. Both implicit and explicit subjects transferred when the egocentric frame was maintained indicating that this representation is common to both processes. Finally, explicit subjects were also able to benefit from the allocentric frame in transfer, which suggests that explicit procedural knowledge may have two tiers comprising egocentric and allocentric representations.     

Neuroscience and eating disorders: the allocentric lock hypothesis

Evidence from psychology and neuroscience indicates that our spatial experience, including the bodily one, involves the integration of different sensory inputs within two different reference frames egocentric (body as reference of first-person experience) and allocentric (body as object in the physical world). Even if functional relations between these two frames are usually limited, they influence each other during the interaction between long- and short-term memory processes in spatial cognition. If, for some reasons, this process is impaired, the egocentric sensory inputs are no more able to update the contents of the allocentric representation of the body: the subject is locked to it. In the presented perspective, subjects with eating disorders are locked to an allocentric representation of their body, stored in long-term memory (allocentric lock). A significant role in the locking may be played by the medial temporal lobe, and in particular by the connection between the hippocampal complex and amygdala. The differences between exogenous and endogenous causes of the lock may also explain the difference between bulimia nervosa and anorexia nervosa.     

Müller-Lyer figures influence the online reorganization of visually guided grasping movements

In advance of grasping a visual object embedded within fins-in and fins-out Müller-Lyer (ML) configurations, participants formulated a premovement grip aperture (GA) based on the size of a neutral preview object. Preview objects were smaller, veridical, or larger than the size of the to-be-grasped target object. As a result, premovement GA associated with the small and large preview objects required significant online reorganization to appropriately grasp the target object. We reasoned that such a manipulation would provide an opportunity to examine the extent to which the visuomotor system engages egocentric and/or allocentric visual cues for the online, feedback-based control of action. It was found that the online reorganization of GA was reliably influenced by the ML figures (i.e., from 20 to 80% of movement time), regardless of the size of the preview object, albeit the small and large preview objects elicited more robust illusory effects than the veridical preview object. These results counter the view that online grasping control is mediated by absolute visual information computed with respect to the observer (e.g., Glover in Behav Brain Sci 27:3-78, 2004; Milner and Goodale in The visual brain in action 1995). Instead, the impact of the ML figures suggests a level of interaction between egocentric and allocentric visual cues in online action control.     

Brain activity associated with recognition of appropriate action selection based on allocentric perspectives

We investigated brain activity associated with recognition of appropriate action selection based on allocentric perspectives using functional magnetic resonance imaging. The participants observed video clips in which one person (responder) passed one of three objects after a request by a second person (requester). The requester was unable to see one of the three objects because it was occluded by another object. Participants were asked to judge the appropriateness of the responder's action selection based on the visual information from the requester's perspective (i.e., allocentric perspective), not the responder's perspective (i.e., egocentric perspective). The experimental factors included the congruency of request interpretation and the appropriateness of action selection. The results showed that brain regions including the right temporo-parieto-occipital (TPO) junction and the left inferior parietal lobule (IPL) were more activated when the interpretation of the requested object differed between the egocentric and allocentric perspectives than when it was the same (the effect of incongruency for consistency). On the other hand, greater activation was found in the right dorsolateral prefrontal cortex (DLPFC) when the incongruency effect was compared only between the conditions of appropriate action selection (the interaction effect). These results suggest that both the TPO junction and IPL are involved in obtaining visual information from the allocentric perspective when visual information based on only the egocentric perspective is insufficient to interpret another person's request. The right DLPFC is likely related to this process to override the interference of action selection based on the egocentric perspective.     

Reference systems for coding spatial information in normal subjects and a deafferented patient

To produce accurate goal-directed arm movements, subjects must determine the precise location of target object. Position of extracorporeal objects can be determined using: (a) an egocentric frame of reference, in which the target is localized in relation to the position of the body; and/or (b) an allocentric system, in which target position is determined in relation to stable visual landmarks surrounding the target (Bridgeman 1989; Paillard 1991). The present experiment was based on the premise that (a) the presence of a structured visual environment enables the use of an allocentric frame of reference, and (b) the sole presence of a visual target within a homogeneous background forces the registration of the target location by an egocentric system. Normal subjects and a deafferented patient (i.e., with an impaired egocentric system) pointed to visual targets presented in both visual environments to evaluate the efficiency of the two reference systems. For normals, the visual environment conditions did not affect pointing accuracy. However, kinematic parameters were affected by the presence or absence of a structured visual surrounding. For the deafferented patient, the presence of a structured visual environment permitted a decrease in spatial errors when compared with the unstructured surrounding condition (for movements with or without visual feedback of the trajectory). Overall, results support the existence of an egocentric and an allocentric reference system capable of organizing extracorporeal space during arm movements directed toward visual targets.     

Deficit in the water-maze after lesions in the anteromedial extrastriate cortex in rats.

The Morris water-maze task was used to evaluate the role of the anteromedial extrastriate visual cortex in the processing of visuospatial information in rats. Six gray male rats received bilateral ibotenic acid injections targeted stereotactically to the rostral part of the anteromedial extrastriate visual cortex. These operated subjects and six other unoperated control rats were tested in the maze. Histological analysis confirmed the localization, symmetry, and depth of lesions in the rostral part of anteromedial area (AMa) in the operated subjects. In these animals, a significantly greater latency to reach the submerged platform was found (U = 0, p = 0.004). The Morris water-maze may be considered as a reference memory task. It presents a stronger demand on the use of allocentric spatial visual cues than on the use of egocentric cues for navigation. Therefore, the present data lend support to the participation of area AMa in the integration of allocentric visuospatial cues or as a link in the memory system involved in the acquisition of this task.     

Altered navigational strategy use and visuospatial deficits in hAPP transgenic mice

Navigation deficits are prominent in Alzheimer's disease (AD) patients and transgenic mice expressing familial AD-mutant hAPP and A beta peptides. To determine the impact of strategy use on these deficits, we assessed hAPP and nontransgenic mice in a cross maze that can be solved by allocentric (world-based) or egocentric (self-based) strategies. Most nontransgenic mice used allocentric strategies, whereas half of hAPP mice were egocentric. At 3 months, all mice learned the cross maze rapidly; at 6 months, only allocentric hAPP mice were impaired. At 3 and 6 months, hAPP mice had reduced hippocampal Fos expression, which correlated with cross maze learning in older mice. Striatal pCREB expression was unaltered in hAPP mice, suggesting striatal sparing. We conclude that egocentric strategy use may be an earlier indicator of hAPP/A beta-induced hippocampal impairment than spatial learning deficits. Persistent use of allocentric strategies when egocentric strategies are available is maladaptive when there is hippocampal damage. Interventions promoting flexibility in selecting learning strategies might help circumvent otherwise debilitating navigational deficits caused by AD-related hippocampal dysfunction.     

Double dissociation of egocentric and allocentric space following medial prefrontal and parietal cortex lesions in the rat

Animals with medial prefrontal cortex or parietal cortex lesions and sham-operated and non-operated controls were tested for the acquisition of an adjacent arm task that accentuated the importance of egocentric spatial localization and a cheese board task that accentuated the importance of allocentric spatial localization. Results indicated that relative to controls, animals with medial-prefrontal cortex lesions are impaired on the adjacent arm task but displayed facilitation on the cheese board task. In contrast, relative to controls, rats with parietal cortex lesions are impaired on the cheese board task but show no impairment on the adjacent arm task. The data suggest a double dissociation of function between medial prefrontal cortex and parietal cortex in terms of coding of egocentric versus allocentric spatial information.     

The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study

The spatial location of an object can be represented in the brain with respect to different classes of reference frames, either relative to or independent of the subject's position. We used functional magnetic resonance imaging to identify regions of the healthy human brain subserving mainly egocentric or allocentric (object-based) coordinates by asking subjects to judge the location of a visual stimulus with respect to either their body or an object. A color-judgement task, matched for stimuli, difficulty, motor and oculomotor responses, was used as a control. We identified a bilateral, though mainly right-hemisphere based, fronto-parietal network involved in egocentric processing. A subset of these regions, including a much less extensive unilateral, right fronto-parietal network, was found to be active during object-based processing. The right-hemisphere lateralization and the partial superposition of the egocentric and the object-based networks is discussed in the light of neuropsychological findings in brain-damaged patients with unilateral spatial neglect and of neurophysiological studies in the monkey.