Eye-Movements During Navigation in a Virtual Tunnel

Eye movements were investigated amongst participants who preferentially use an egocentric or an allocentric frame of reference during navigation through computer simulated tunnels. Performance was highly accurate even though the tunnel passages contained only sparse visual flow and no differences in homing accuracy between subjects using one or the other reference frame was observed. Analyses of eye-movements revealed that gaze was centered on the tunnel's visual centroid during straight segments. However, during turns mean gaze position was directed toward the outer wall. As the angle of turn increased, the prevalence of overall eye movements and the laterality of gaze were greater than during turns of lesser angle. Even though the strategy groups reacted based on distinct reference frames, comparable patterns of eye movements were revealed for both strategies. The data describe how information during navigation through sparse visual environments is selected and demonstrate that the preferential use of an egocentric or an allocentric frame of reference is independent of eye-movement patterns. Thus, a purely cognitive basis for individual differences in reference frame usage can be assumed.     

Frames of reference for eye–head gaze shifts evoked during frontal eye field stimulation

The frontal eye field (FEF), in the prefrontal cortex, participates in the transformation of visual signals into saccade motor commands and in eye–head gaze control. The FEF is thought to show eye‐fixed visual codes in head‐restrained monkeys, but it is not known how it transforms these inputs into spatial codes for head‐unrestrained gaze commands. Here, we tested if the FEF influences desired gaze commands within a simple eye‐fixed frame, like the superior colliculus (SC), or in more complex egocentric frames like the supplementary eye fields (SEFs). We electrically stimulated 95 FEF sites in two head‐unrestrained monkeys to evoke 3D eye–head gaze shifts and then mathematically rotated these trajectories into various reference frames. In theory, each stimulation site should specify a specific spatial goal when the evoked gaze shifts are plotted in the appropriate frame. We found that these motor output frames varied site by site, mainly within the eye‐to‐head frame continuum. Thus, consistent with the intermediate placement of the FEF within the high‐level circuits for gaze control, its stimulation‐evoked output showed an intermediate trend between the multiple reference frame codes observed in SEF‐evoked gaze shifts and the simpler eye‐fixed reference frame observed in SC‐evoked movements. These results suggest that, although the SC, FEF and SEF carry eye‐fixed information at the level of their unit response fields, this information is transformed differently in their output projections to the eye and head controllers.     

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).     

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).     

The dependencies of fronto‐parietal BOLD responses evoked by covert visual search suggest eye‐centred coding

Visual scenes explored covertly are initially represented in a retinal frame of reference (FOR). On the other hand, ‘later’ stages of the cortical network allocating spatial attention most probably use non‐retinal or non‐eye‐centred representations as they may ease the integration of different sensory modalities for the formation of supramodal representations of space. We tested if the cortical areas involved in shifting covert attention are based on eye‐centred or non‐eye‐centred coding by using functional magnetic resonance imaging. Subjects were scanned while detecting a target item (a regularly oriented ‘L’) amidst a set of distractors (rotated ‘L's). The array was centred either 5° right or left of the fixation point, independent of eye‐gaze orientation, the latter varied in three steps: straight relative to the head, 10° left or 10° right. A quantitative comparison of the blood‐oxygen‐level‐dependent (BOLD) responses for the three eye‐gaze orientations revealed stronger BOLD responses in the right intraparietal sulcus (IPS) and the right frontal eye field (FEF) for search in the contralateral (i.e. left) eye‐centred space, independent of whether the array was located in the right or left head‐centred hemispace. The left IPS showed the reverse pattern, i.e. an activation by search in the right eye‐centred hemispace. In other words, the IPS and the right FEF, members of the cortical network underlying covert search, operate in an eye‐centred FOR.     

The egocentric spatial reference frame used in dorsal-lateral prefrontal working memory in primates

The dorsal-lateral prefrontal cortex (dlPFC) has been proposed to be the site of spatial working memory (WM), and this concept has had a profound influence on functional studies of the prefrontal cortex (PFC). The concept of spatial WM has been understood to mean that the location of an object is memorized for a short period of time. However, this concept of space is a simplification. To process the spatial information, different spatial frames can be used. In this review, the authors present data from their own laboratory to argue that the dlPFC is related to the egocentric spatial information processing (ESIP) in WM. The goal of this review is to introduce and discuss the egocentric spatial reference frame (ESRF) located in the dlPFC. The ESIP in the PFC might be involved in self-recognition.     

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

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

The neural basis of ego- and allocentric reference frames in spatial navigation: evidence from spatio-temporal coupled current density reconstruction

Different strategies in spatial navigation during passages through computer-simulated tunnels were investigated by means of EEG source reconstruction. The tunnels consisted of straight and curved segments and provided only visual flow, but no landmark, information. At the end of each tunnel passage, subjects had to indicate their end position relative to the starting point of the tunnel. Even though the visual information was identical for all subjects, two different strategy groups were identified: one group using an egocentric and the other group an allocentric reference frame. The current density reconstruction revealed the use of one or the other reference frame to be associated with distinct cortical activation patterns during critical stages of the task. For both strategy groups, an occipito-temporal network was dominantly active during the initial, straight tunnel segment. With turns in the tunnel, however, the activation patterns started to diverge, reflecting translational and/or rotational changes in the underlying coordinate systems. Computation of an egocentric reference frame was associated with prevailing activity within a posterior parietal-premotor network, with additional activity in frontal areas. In contrast, computation of an allocentric reference frame was associated with dominant activity within an occipito-temporal network, confirming right-temporal structures to play a crucial role for an allocentric representation of space.     

Both egocentric and allocentric cues support spatial priming in visual search

The perception-action model proposes that vision for perception and vision for action are subserved by two separate cortical systems, the ventral and dorsal streams, respectively [Milner, A. D., & Goodale, M. A. (1995). The visual brain in action (1st ed.). Oxford: Oxford University Press; Milner, A. D., & Goodale, M. A. (2006). The visual brain in action (2nd ed.). Oxford: Oxford University Press Inc.]. The dorsal stream codes spatial information egocentrically, that is, relative to the observer. Egocentric representations are argued to be highly transient; therefore, it might be expected that egocentric information cannot be used for spatial memory tasks, even when the visual information only needs to be retained for a few seconds. Here, by applying a spatial priming paradigm to a visual search task, we investigated whether short-term spatial memory can use egocentric information. Spatial priming manifests itself in speeded detection times for a target when that target appears in the same location it previously appeared in. Target locations can be defined in either egocentric or allocentric (i.e. relative to other items in the display) frames of reference; however, it is unclear which of these are used in spatial priming, or if both are. Our results show that both allocentric and egocentric cues were used in spatial priming, and that egocentric cues were in fact more effective than allocentric cues for short-term priming. We conclude that egocentric information can persist for several seconds; a conclusion which is at odds with the assumption of the perception-action model that egocentric representations are highly transient.     

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.     

Patterns of bimanual interference reveal movement encoding within a radial egocentric reference frame

Constraints on interlimb coordination have been studied intensively in past years with a primary focus on temporal features. The present study addressed spatial constraints or the degree of directional interference as a function of different line combinations between the upper limbs as well as the modulation of this interference as a result of different board orientations within the performer's workspace. This paradigm was used to address a prominent theme in motor neuroscience, namely whether (bimanual) movements are encoded within an allocentric reference frame (pattern of interference invariant with respect to extrinsic space) or within an egocentric reference frame (pattern of interference invariant relative to the center of the performer's action space, i.e., intrinsic). The observed patterns of interference revealed that movements are primarily encoded within a radial egocentric reference frame in which the performer is the center of action space. The present psychophysical findings converge with primate single-cell recording studies in which the direction has been identified as a primary movement parameter that is encoded in various brain regions, thereby constituting a principal determinant of bilateral interference.     

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 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.     

Impaired passive maintenance and spared manipulation of internal representations in patients with schizophrenia

Working memory (WM) impairment is a core feature of schizophrenia (SZ), but the integrity of the various components of WM is unclear. After encoding, mental representations must be maintained in WM during the delay period. In addition to maintenance, manipulation of internal representation can occur in WM. It has been argued that manipulation of items in WM is more impaired than simple maintenance in SZ, but direct empirical data to support this claim have been mixed. Discrepant findings among studies might be explained by task parameters, specifically the degree to which the manipulation task places demands on encoding and maintenance processes. The present study set out to examine these components of WM in patients with SZ (n = 20) and demographically matched healthy controls (n = 19) using a spatial delayed response task (DRT) to measure maintenance processes and 2 mental rotation tasks (allocentric and egocentric) with no delay period or restriction on encoding time to measure manipulation processes. Consistent with previous findings, patients were impaired on the spatial DRT. However, patients performed equally well on the egocentric mental rotation task and were more accurate than controls on the allocentric mental rotation task as the required degree of rotation increased. These results indicated impaired maintenance and spared manipulation of representations in WM and suggest a pocket of cognitive function that might be enhanced in SZ.     

Parietal blood oxygenation level‐dependent response evoked by covert visual search reflects set‐size effect in monkeys

Distinguishing a target from distractors during visual search is crucial for goal‐directed behaviour. The more distractors that are presented with the target, the larger is the subject's error rate. This observation defines the set‐size effect in visual search. Neurons in areas related to attention and eye movements, like the lateral intraparietal area (LIP) and frontal eye field (FEF), diminish their firing rates when the number of distractors increases, in line with the behavioural set‐size effect. Furthermore, human imaging studies that have tried to delineate cortical areas modulating their blood oxygenation level‐dependent (BOLD) response with set size have yielded contradictory results. In order to test whether BOLD imaging of the rhesus monkey cortex yields results consistent with the electrophysiological findings and, moreover, to clarify if additional other cortical regions beyond the two hitherto implicated are involved in this process, we studied monkeys while performing a covert visual search task. When varying the number of distractors in the search task, we observed a monotonic increase in error rates when search time was kept constant as was expected if monkeys resorted to a serial search strategy. Visual search consistently evoked robust BOLD activity in the monkey FEF and a region in the intraparietal sulcus in its lateral and middle part, probably involving area LIP. Whereas the BOLD response in the FEF did not depend on set size, the LIP signal increased in parallel with set size. These results demonstrate the virtue of BOLD imaging in monkeys when trying to delineate cortical areas underlying a cognitive process like visual search. However, they also demonstrate the caution needed when inferring neural activity from BOLD activity.     

Object-based neglect varies with egocentric position

Different reference frames have been identified to influence neglect behavior. In particular, neglect has been demonstrated to be related to the contralesional side of the subject's body (egocentric reference frames) as well as to the contralesional side of individual objects irrespective of their position to the patient (object-based reference frame). There has been discussion whether this distinction separates neglect into body- and object-based forms. The present experiment aimed to prove possible interactions between object-based and egocentric aspects in spatial neglect. Neglect patients' eye and head movements were recorded while they explored objects at five egocentric positions along the horizontal dimension of space. The patients showed both egocentric as well as object-based behavior. Most interestingly, data analysis revealed that object-based neglect varied with egocentric position. Although the neglect of the objects' left side was strong at contralesional egocentric positions, it ameliorated at more ipsilesional egocentric positions of the objects. The patients showed steep, ramp-shaped patterns of exploration for objects located on the far contralesional side and a broadening of these patterns as the locations of the objects shifted more to the ipsilesional side. The data fitted well with the saliency curves predicted by a model of space representation, which suggests that visual input is represented in two modes simultaneously: in veridical egocentric coordinates and in within-object coordinates.     

Opposite visual field asymmetries for egocentric and allocentric spatial judgments

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

Do parietal cortical lesions impair spatial attention or allocentric spatial perception?

It remains unclear whether monkeys with large parietal cortical lesions fail "landmark" tasks because they cannot judge the relative distances between landmark and response locations, or because they fail to attend to, or even to notice, the landmark. Monkeys with small posterior parietal (SPP), large posterior parietal (LPP), superior temporal sulcus (STS), or frontal eye field (FEF) lesions were tested on a landmark task in which the physical salience of the landmark and its location varied. Only the LPP monkeys were impaired, seemingly because they overtly failed to shift attention during each trial, responding to whichever food well they looked at first. A task based on one used with neurological patients was therefore introduced in which the monkeys had to discriminate between two white square plaques each containing a spot, where the spot on the positive stimulus was centrally placed. Solving this task requires an allocentric judgement about the relative location of each spot to the edges of the plaque. Even on the most difficult discrimination, monkeys with large parietal lobe lesions were unimpaired. The deficits previously reported on landmark tasks probably reflect a failure of spatial attention or attention to objects rather than an inability to judge allocentric spatial relationships.     

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.