Allocentric Representations Research Articles

The Simon effect based on the egocentric and allocentric reference frame.

The classic Simon effect refers to the phenomenon that responses are faster when the task-irrelevant egocentric stimulus location is on the same side as the response hand than when not. However, the spatial location of an object often varies according to which reference frame the object location was represented in, e.g., egocentric versus allocentric reference frame. It has been unknown, however, whether and how the Simon effect based on the egocentric and the allocentric reference interact, and whether the potential interaction between them is affected by task demands. To investigate these questions, we orthogonally crossed the stimulus-response compatibility induced by the egocentric and the allocentric positions during the Simon effect. Moreover, the irrelevant egocentric and allocentric positions were either explicitly represented via interleaving spatial and non-spatial tasks in Experiment 1 or not in Experiment 2. The results suggested that the Simon effect based on the egocentric locations occurred irrespective of whether the egocentric representations were explicitly coded based on current task demands or not. The Simon effect based on allocentric locations, however, seemed to occur only when the allocentric representations were explicitly induced. Moreover, the egocentric and allocentric Simon effect interacted in a similar way irrespective of task demands, with significantly delayed responses when both the egocentric and the allocentric locations were incongruent with the response code.

Context influences spatial frames of reference in bonobos (Pan paniscus)

Primates must solve complex spatial problems when foraging, such as finding patchy resources and navigating between different locations. However, the nature of the cognitive representations supporting these types of behaviors is currently unclear. In humans, there has been great debate concerning the relative importance of egocentric representations (which are viewer-dependent) versus allocentric representations (which are based on aspects of the external environment). Comparative studies of nonhuman apes can illuminate which aspects of human spatial cognition are shared with other primates, versus which aspects are unique to our lineage. The current studies therefore examined spatial cognitive development in one of our closest living relatives, bonobos (Pan paniscus) across contexts. The first study assessed how younger bonobos encode locations in a place-response task in which apes first learn that one of two locations is consistently baited with a reward, and then must approach the two locations from a flipped perspective. The second study examined how a larger age sample of bonobos responded to a spatial relations task in which they first experience that one location is baited, and then can generalize this learning to a new set of targets. Results indicated that while bonobos exhibited a predominantly allocentric strategy in the first study, they consistently exhibited an egocentric strategy in the second. Together, these results show that bonobos can use both strategies to encode spatial information, and illuminate the complementary contributions to cognition made by egocentric and allocentric representations.

Human place and response learning: navigation strategy selection, pupil size and gaze behavior

In this study, we examined the cognitive processes and ocular behavior associated with on-going navigation strategy choice using a route learning paradigm that distinguishes between three different wayfinding strategies: an allocentric place strategy, and the egocentric associative cue and beacon response strategies. Participants approached intersections of a known route from a variety of directions, and were asked to indicate the direction in which the original route continued. Their responses in a subset of these test trials allowed the assessment of strategy choice over the course of six experimental blocks. The behavioral data revealed an initial maladaptive bias for a beacon response strategy, with shifts in favor of the optimal configuration place strategy occurring over the course of the experiment. Response time analysis suggests that the configuration strategy relied on spatial transformations applied to a viewpoint-dependent spatial representation, rather than direct access to an allocentric representation. Furthermore, pupillary measures reflected the employment of place and response strategies throughout the experiment, with increasing use of the more cognitively demanding configuration strategy associated with increases in pupil dilation. During test trials in which known intersections were approached from different directions, visual attention was directed to the landmark encoded during learning as well as the intended movement direction. Interestingly, the encoded landmark did not differ between the three navigation strategies, which is discussed in the context of initial strategy choice and the parallel acquisition of place and response knowledge.

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.

Gravity influences the visual representation of object tilt in parietal cortex.

Sensory systems encode the environment in egocentric (e.g., eye, head, or body) reference frames, creating inherently unstable representations that shift and rotate as we move. However, it is widely speculated that the brain transforms these signals into an allocentric, gravity-centered representation of the world that is stable and independent of the observer's spatial pose. Where and how this representation may be achieved is currently unknown. Here we demonstrate that a subpopulation of neurons in the macaque caudal intraparietal area (CIP) visually encodes object tilt in nonegocentric coordinates defined relative to the gravitational vector. Neuronal responses to the tilt of a visually presented planar surface were measured with the monkey in different spatial orientations (upright and rolled left/right ear down) and then compared. This revealed a continuum of representations in which planar tilt was encoded in a gravity-centered reference frame in approximately one-tenth of the comparisons, intermediate reference frames ranging between gravity-centered and egocentric in approximately two-tenths of the comparisons, and in an egocentric reference frame in less than half of the comparisons. Altogether, almost half of the comparisons revealed a shift in the preferred tilt and/or a gain change consistent with encoding object orientation in nonegocentric coordinates. Through neural network modeling, we further show that a purely gravity-centered representation of object tilt can be achieved directly from the population activity of CIP-like units. These results suggest that area CIP may play a key role in creating a stable, allocentric representation of the environment defined relative to an "earth-vertical" direction.

A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective.

While the widely studied allocentric spatial representation holds a special status in neuroscience research, its exact nature and neural underpinnings continue to be the topic of debate, particularly in humans. Here, based on a review of human behavioral research, we argue that allocentric representations do not provide the kind of map-like, metric representation one might expect based on past theoretical work. Instead, we suggest that almost all tasks used in past studies involve a combination of egocentric and allocentric representation, complicating both the investigation of the cognitive basis of an allocentric representation and the task of identifying a brain region specifically dedicated to it. Indeed, as we discuss in detail, past studies suggest numerous brain regions important to allocentric spatial memory in addition to the hippocampus, including parahippocampal, retrosplenial, and prefrontal cortices. We thus argue that although allocentric computations will often require the hippocampus, particularly those involving extracting details across temporally specific routes, the hippocampus is not necessary for all allocentric computations. We instead suggest that a non-aggregate network process involving multiple interacting brain areas, including hippocampus and extra-hippocampal areas such as parahippocampal, retrosplenial, prefrontal, and parietal cortices, better characterizes the neural basis of spatial representation during navigation. According to this model, an allocentric representation does not emerge from the computations of a single brain region (i.e., hippocampus) nor is it readily decomposable into additive computations performed by separate brain regions. Instead, an allocentric representation emerges from computations partially shared across numerous interacting brain regions. We discuss our non-aggregate network model in light of existing data and provide several key predictions for future experiments.

Examining the role of the temporo-parietal network in memory, imagery, and viewpoint transformations.

The traditional view of the medial temporal lobe (MTL) focuses on its role in episodic memory. However, some of the underlying functions of the MTL can be ascertained from its wider role in supporting spatial cognition in concert with parietal and prefrontal regions. The MTL is strongly implicated in the formation of enduring allocentric representations (e.g., O'Keefe, 1976; King et al., 2002; Ekstrom et al., 2003). According to our BBB model (Byrne et al., 2007), these representations must interact with head-centered and body-centered representations in posterior parietal cortex via a transformation circuit involving retrosplenial areas. Egocentric sensory representations in parietal areas can then cue the recall of allocentric spatial representations in long-term memory and, conversely, the products of retrieval in MTL can generate mental imagery within a parietal “window.” Such imagery is necessarily egocentric and forms part of visuospatial working memory, in which it can be manipulated for the purpose of planning/imagining the future. Recent fMRI evidence (Lambrey et al., 2012; Zhang et al., 2012) supports the BBB model. To further test the model, we had participants learn the locations of objects in a virtual scene and tested their spatial memory under conditions that impose varying demands on the transformation circuit. We analyzed how brain activity correlated with accuracy in judging the direction of an object (1) from visuospatial working memory (we assume transient working memory due to the order of tasks and the absence of change in viewpoint, but long-term memory retrieval is also possible), (2) after a rotation of viewpoint, or (3) after a rotation and translation of viewpoint (judgment of relative direction). We found performance-related activity in both tasks requiring viewpoint rotation (ROT and JRD, i.e., conditions 2 and 3) in the core medial temporal to medial parietal circuit identified by the BBB model. These results are consistent with the predictions of the BBB model, and shed further light on the neural mechanisms underlying spatial memory, mental imagery and viewpoint transformations.

Allocentric versus egocentric representation of remembered reach targets in human cortex.

The location of a remembered reach target can be encoded in egocentric and/or allocentric reference frames. Cortical mechanisms for egocentric reach are relatively well described, but the corresponding allocentric representations are essentially unknown. Here, we used an event-related fMRI design to distinguish human brain areas involved in these two types of representation. Our paradigm consisted of three tasks with identical stimulus display but different instructions: egocentric reach (remember absolute target location), allocentric reach (remember target location relative to a visual landmark), and a nonspatial control, color report (report color of target). During the delay phase (when only target location was specified), the egocentric and allocentric tasks elicited widely overlapping regions of cortical activity (relative to the control), but with higher activation in parietofrontal cortex for egocentric task and higher activation in early visual cortex for allocentric tasks. In addition, egocentric directional selectivity (target relative to gaze) was observed in the superior occipital gyrus and the inferior occipital gyrus, whereas allocentric directional selectivity (target relative to a visual landmark) was observed in the inferior temporal gyrus and inferior occipital gyrus. During the response phase (after movement direction had been specified either by reappearance of the visual landmark or a pro-/anti-reach instruction), the parietofrontal network resumed egocentric directional selectivity, showing higher activation for contralateral than ipsilateral reaches. These results show that allocentric and egocentric reach mechanisms use partially overlapping but different cortical substrates and that directional specification is different for target memory versus reach response.

Allocentric but not egocentric orientation is impaired during normal aging: an ERP study.

Behavioral studies of spatial navigation in aging indicate that orientation using an allocentric reference frame (object-centered orientation) is impaired, whereas orientation using egocentric processes (self-centered orientation) is not. It has been proposed that navigational deficits may result from more general alterations of perception and attention or executive functions. The purpose of this study is to assess allocentric and egocentric representation in elderly individuals, and to determine if age-related deficits in spatial navigation are related to an attentional decline. We assessed encoding of the position of geometrical shapes, depending specifically on an allocentric or egocentric reference frame, during ERP recording in young and old subjects. Aging was associated with a performance decline in allocentric, but not egocentric, encoding. Both allocentric and egocentric conditions elicited parietal early components P1 and N1, reflecting top-down modulation, and components P2 and N2, reflecting selective attention and stimulus categorization. We observed age-associated effects on N1 and N2 amplitudes and on N2 latency in both spatial conditions. Moreover, impaired allocentric performance in older subjects was associated with a greater P2 amplitude and delayed P2 latency compared with younger subjects. These results suggest that elderly individuals present with deficits when spatial orientation relies on allocentric representation, and are associated with age-related deficits in spatial attention.

Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition.

Spatial navigation requires memory representations of landmarks and other navigation cues. The retrosplenial cortex (RSC) is anatomically positioned between limbic areas important for memory formation, such as the hippocampus (HPC) and the anterior thalamus, and cortical regions along the dorsal stream known to contribute importantly to long-term spatial representation, such as the posterior parietal cortex. Damage to the RSC severely impairs allocentric representations of the environment, including the ability to derive navigational information from landmarks. The specific deficits seen in tests of human and rodent navigation suggest that the RSC supports allocentric representation by processing the stable features of the environment and the spatial relationships among them. In addition to spatial cognition, the RSC plays a key role in contextual and episodic memory. The RSC also contributes importantly to the acquisition and consolidation of long-term spatial and contextual memory through its interactions with the HPC. Within this framework, the RSC plays a dual role as part of the feedforward network providing sensory and mnemonic input to the HPC and as a target of the hippocampal-dependent systems consolidation of long-term memory.

Does blindness affect egocentric and allocentric frames of reference in small and large scale spaces?

There is evidence that early deprivation of vision prompts the use of body-based, egocentric spatial representations in congenitally blind individuals, whereas previous visual experience favors the use of object-based, allocentric representations (e.g. Pasqualotto A, Spiller MJ, Jansari AS, Proulx MJ. Visual experience facilitates allocentric spatial representation. Behav Brain Res 2013;236:175–79). Here we investigated whether the influence of the visual status on the capacity to represent egocentric and allocentric spatial relations is mediated by the scale of space explored: large-scale (where a haptic+locomotor exploration is required) and small-scale space (where haptic exploration is needed). Our results showed that congenitally blind people had more difficulty in representing spatial information allocentrically with respect to late blind and sighted individuals, but this difficulty was stronger with large-scale than small-scale space. Instead, egocentric performance was better than the allocentric one for all groups, particularly in the small scale condition. These results suggest that visual experience is necessary to develop accurate allocentric representations especially of large-scale spaces. This is probably due to its capacity to convey a large amount of spatial information simultaneously and to its role on the setting up of multisensory brain areas underlying spatial cognition. In the absence of any kind of visual experience, egocentric spatial representations are favored, especially in small-scale space, when the body offers a stable anchor point.

Episodic Memory as Re-Experiential Memory: Kantian, Developmental, and Neuroscientific Currents

Recent work on the early development of episodic memory in my laboratory has been fuelled by the following assumption: if episodic memory is re-experiential memory then Kant’s analysis of the spatiotemporal nature of experience should constrain and positively influence theories of episodic memory development. The idea is that re-experiential memory will “inherit” these spatiotemporal features. On the basis of this assumption, Russell and Hanna (Mind and Language 27(1):29–54, 2012) proposed that (a) the spatial element of re-experience is egocentric and (b) that the temporal element of re-experiencing involves order/simultaneity. The first of these assumptions is immediately problematic for two reasons. In the first place, if we assume that early episodic recall mediated by processing in the hippocampus, then (a) is clearly in tension with the fact that spatial coding in the hippocampus is allocentric/environment-centred. Second, two of our own recent experiments (described here) show that when only egocentric cues are available in a What/When/Where episodic memory task it is not possible to distinguish young children’s performance from semantic memory. I argue that this tension should be resolved by recognising that the egocentric coding of the original experience as being of an objective scene relies upon allocentric representations and these are preserved in re-experiential memory, allowing a recollection of the objective nature of the scene on which one takes a subjective view.

Egocentric representations of space co-exist with allocentric representations: Evidence from spatial neglect

The brain transforms sensory input to motor coordinates to accommodate for changes of posture and gaze direction. Neurophysiological and neuropsychological evidence supports the existence of multiple representations of space. A debated issue regards whether objects that we see are encoded in egocentric frames only or also maintain an object-centered frame of reference. Previous clinical studies were unable to discriminate between these models as the stimuli used to determine object-based (allocentric) biases are contaminated by body-centered (egocentric) effects. To address this, we used stimuli where allocentric side was elicited by gestalt configuration rather than egocentric location. We then displayed these stimuli at different egocentric positions allowing us to independently measure the effects of allocentric position, egocentric position as well as their interaction. In a group of stroke patients with neglect we demonstrate that allocentric biases are modulated as a function of egocentric position. These findings help adjudicate between the different models of space representation, demonstrating that specific allocentric deficits not only exist but also often co-exist with egocentric biases.

What is the role of spatial processing in the decline of episodic memory in Alzheimer's disease? The "mental frame syncing" hypothesis.

The current theories on episodic memory suggest a crucial role of spatial processing for an effective retrieval. For a successful episodic recall, the long-term allocentric scene has to be translated into an egocentric scene. Here, we argue that a crucial role for an episodic retrieval is played by a “mental frame syncing” between two kinds of allocentric representations. This neurocognitive process allows an effective retrieval of our past experiences by synchronizing the allocentric view-point independent representation with the allocentric view-point dependent representation. If the “mental frame syncing” stops, even momentarily, it is difficult to reconstruct a coherent spatial scaffold upon which to effectively retrieve our previous events within an egocentric perspective. This is what apparently happens in Alzheimer’s disease: a break in the “mental frame syncing” between these two kinds of allocentric representations, underpinned by damage to the hippocampus, may contribute significantly to the early deficit in episodic memory.

How Optic Flow and Inertial Cues Improve Motion Perception.

Estimating our egocentric heading direction is an important component of navigation. Recent studies have explored how inertial cues from the vestibular system and optic flow signals from the visual system interact to improve perceptual precision and accuracy. Heading precision is improved through multisensory integration, whereas heading accuracy is maintained through multisensory calibration mechanisms. Neural correlates of these behaviors are found in a large interconnected cortical network, although the specific contributions of each area remain to be explored. Whether and how this multisensory self-motion cortical circuit contributes to navigation and how egocentric heading signals interact with the allocentric representations for foraging and exploration also remain challenges for the future.

An Active System for Visually-Guided Reaching in 3D across Binocular Fixations

Based on the importance of relative disparity between objects for accurate hand-eye coordination, this paper presents a biological approach inspired by the cortical neural architecture. So, the motor information is coded in egocentric coordinates obtained from the allocentric representation of the space (in terms of disparity) generated from the egocentric representation of the visual information (image coordinates). In that way, the different aspects of the visuomotor coordination are integrated: an active vision system, composed of two vergent cameras; a module for the 2D binocular disparity estimation based on a local estimation of phase differences performed through a bank of Gabor filters; and a robotic actuator to perform the corresponding tasks (visually-guided reaching). The approach's performance is evaluated through experiments on both simulated and real data.

Functional neuro-anatomy of egocentric versus allocentric space representation

The functional neuroanatomy of the egocentric and allocentric representations of space remains poorly studied with neuroimaging. Here we aim to determine brain structures subserving two different kinds of spatial representations centred on the main axis of either the body or the external scene. Sixteen healthy participants evaluated the alignment of a bar relative to the middle of their body (Ego) or relative to another stimulus (Allo) during functional MRI. In a control task (Ctrl), they had to judge the colour of the bar. Correct response rates and response times were similar in the three tasks. fMRI data revealed a predominant role of the right hemisphere in the egocentric task (Ego vs. Allo): selective activity was found in the occipital, superior parietal, and inferior frontal cortices, as well as in the precuneus and supplementary motor area. On the left side, the insula, thalamus, and cerebellum were also activated. Conversely, the allocentric task (Allo vs. Ctrl) showed selective activity centred on the left temporal gyrus. This study demonstrates a right hemisphere dominance for representations centred on the longitudinal body axis, but more left-sided activity for scene/object-centred representations of space. These new data shed light on the unique role of several regions involved in spatial perception and help better understand spatial deficits in patients with right hemispheric lesions.

Place-related neuronal activity in the monkey parahippocampal gyrus and hippocampal formation during virtual navigation

Neuropsychological data in primates demonstrated a pivotal role of the hippocampal formation (HF) and parahippocampal gyrus (PH) in navigation and episodic memory. To investigate the role of HF and PH neurons in environmental scaling in primates, we recorded neuronal activities in the monkey HF and PH during virtual navigation (VN) and pointer translocation (PT) tasks. The monkeys had to navigate within three differently sized virtual spaces with the same spatial cues (VN task) or move a pointer on a screen (PT task) by manipulating a joystick to receive a reward. Of the 234 recorded neurons, 170 and 61 neurons displayed place-related activities in the VN and PT tasks, respectively. Significant differences were observed between the HF and PH neurons. The spatial similarity of place fields between the two different virtual spaces was lower in PH than in HF, while specificities of the neuronal responses to distal spatial cues were higher in PH than in HF. Spatial view information was predominately processed in posterior PH. The spatial scales (place field sizes) of the HF and PH neurons were reduced in the reduced virtual space, as shown in rodent place cells. These results suggest the complementary roles of HF (allocentric representation of landmarks) and PH (representation of the spatial layout of landmarks) in the recognition of a location during navigation.

The complex interplay between three-dimensional egocentric and allocentric spatial representation

Jeffery et al. characterize the egocentric/allocentric distinction as discrete. But paradoxically, much of the neural and behavioral evidence they adduce undermines a discrete distinction. More strikingly, their positive proposal - the bicoded map hypothesis - reflects a more complex interplay between egocentric and allocentric coding than they acknowledge. Properly interpreted, their proposal about three-dimensional spatial representation contributes to recent work on embodied cognition.

Making our ends meet: shared intention, goal adoption and the third-person perspective

Mind reading (i.e. the ability to infer the mental state of another agent) is taken to be the main cognitive ability required to share an intention and to collaborate. In this paper, I argue that another cognitive ability is also necessary to collaborate: representing others’ and ones’ own goals from a third-person perspective (other-centred or allocentric representation of goals). I argue that allocentric mind reading enables the cognitive ability of goal adoption, i.e. having the goal that another agent’s achieve p because and as long as another agent has that goal that p. Having clarified the relevance of mutual goal adoption for acting jointly, I argue that when an intention is shared between several agents, each individual has an intention in favour of the joint action and one in favour of a joint mode of reasoning. This mode of reasoning is allocentric reasoning. Finally, I elaborate on the consequences of this view for the scientific study of human collaboration.