Dissociation of egocentric and allocentric spatial processing in prefrontal cortex

Monkeys with lesions of areas 9 and 46 performed three variants of the spatial delayed response (SDR) task. There were no impairments in allocentric spatial memory in which geometrical relationships between environmental cues were used to identify spatial location; thus, memory of a 3D environmental map is intact. In contrast, there were severe impairments in egocentric spatial memory guided by visual or tactile cues that monkeys can relate to their viewing perspective during testing. These results strongly suggest that dorsolateral prefrontal cortex selectively mediates spatial memory tasks that are solved by referencing the location of targets to the body's orientation. (C) 2003 Lippincott Williams Wilkins.

Spatial reference of black capuchin monkeys in Brazilian Atlantic Forest: egocentric or allocentric?

Wild primates occupy large home ranges and travel long distances to reach goals. However, how primates are able to remember goal locations and travel efficiently is unclear. Few studies present consistent results regarding what reference system primates use to navigate, and what kind of spatial information they recognize. We analysed the pattern of navigation of one wild group of black capuchin monkeys, Cebus nigritus, at Atlantic Forest for 100 days in Carlos Botelho State Park (PECB), Brazil. We tested predictions based on the alternative hypotheses that black capuchin monkeys navigate using a sequence of landmarks as an egocentric reference system or an allocentric reference system, or both, depending on availability of food resources. The group location was recorded using a GPS device collecting coordinates at 5 min intervals, and route maps were generated using ArcView v9.3.1. The study group travelled through habitual routes during less than 30% of our study sample, and revisited resources from different starting points, using different paths and routes, even when prominent landmarks near feeding locations were not visible. The study group used habitual routes more frequently when high-quality foods were scarce, and navigated using different paths when revisiting food sources. Results support the hypothesis that black capuchin monkeys at PECB navigate using both egocentric and allocentric systems of reference, depending on the quality and distribution of the food resource they find. (C) 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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.

Allocentric visual cues influence mental transformation of bodies

Identifying a human body stimulus involves mentally rotating an embodied spatial representation of one's body (motoric embodiment) and projecting it onto the stimulus (spatial embodiment). Interactions between these two processes (spatial and motoric embodiment) may thus reveal cues about the underlying reference frames. The allocentric visual reference frame, and hence the perceived orientation of the body relative to gravity, was modulated using the York Tumbling Room, a fully furnished cubic room with strong directional cues that can be rotated around a participant's roll axis. Sixteen participants were seated upright (relative to gravity) in the Tumbling Room and made judgments about body and hand stimuli that were presented in the frontal plane at orientations of 0°, 90°, 180° (upside down), or 270° relative to them. Body stimuli have an intrinsic visual polarity relative to the environment whereas hands do not. Simultaneously the room was oriented 0°, 90°, 180° (upside down), or 270° relative to gravity resulting in sixteen combinations of orientations. Body stimuli were more accurately identified when room and body stimuli were aligned. However, such congruency did not facilitate identifying hand stimuli. We conclude that static allocentric visual cues can affect embodiment and hence performance in an egocentric mental transformation task. Reaction times to identify either hands or bodies showed no dependence on room orientation.

Allocentric spatial performance higher in early-blind and sighted adults than in retinopathy-of-prematurity adults

The question as to whether people totally blind since infancy process allocentric or ‘external’ spatial information like the sighted has caused considerable debate within the literature. Due to the extreme rarity of the population, researchers have often included individuals with Retinopathy of Prematurity (RoP – over oxygenation at birth) within the sample. However, RoP is inextricably confounded with prematurity per se. Prematurity, without visual disability, has been associated with spatial processing difficulties. In this experiment, blindfolded sighted and two groups of functionally totally blind participants heard text descriptions from a survey (allocentric) or route (egocentric) perspective. One blind group lost their sight due to retinopathy of prematurity (RoP – over oxygenation at birth) and a second group before 24 months of age. The accuracy of participants’ mental representations derived from the text descriptions were assessed via questions and maps. The RoP participants had lower scores than the sighted and early blind, who performed similarly. In other words, it was not visual impairment alone that resulted in impaired allocentric spatial performance in this task, but visual impairment together with RoP. This finding may help explain the contradictions within the existing literature on the role of vision in allocentric spatial processing.

Using idiothetic cues to swim a path with a fixed trajectory and distance: Necessary involvement of the hippocampus but not the retrosplenial cortex.

Rats rapidly learned to find a submerged platform in a water maze at a constant distance and angle from the start point, which changed on every trial. The rats performed accurately in the light and dark, but prior rotation disrupted the latter condition. The rats were then retested after receiving cytotoxic hippocampal or retrosplenial cortex lesions. Retrosplenial lesions had no apparent effect in either the light or dark. Hippocampal lesions impaired performance in both conditions but spared the ability to locate a platform placed in the center of the pool. A hippocampal deficit emerged when this pool-center task was run in the dark. The spatial effects of hippocampal damage extend beyond allocentric tasks to include aspects of idiothetic guidance.

Using time-to-contact information to assess potential collision modulates both visual and temporal prediction networks

Accurate estimates of the time-to-contact (TTC) of approaching objects are crucial for survival. We used an ecologically valid driving simulation to compare and contrast the neural substrates of egocentric (head-on approach) and allocentric (lateral approach) TTC tasks in a fully factorial, event-related fMRI design. Compared to colour control tasks, both egocentric and allocentric TTC tasks activated left ventral premotor cortex/frontal operculum and inferior parietal cortex, the same areas that have previously been implicated in temporal attentional orienting. Despite differences in visual and cognitive demands, both TTC and temporal orienting paradigms encourage the use of temporally predictive information to guide behaviour, suggesting these areas may form a core network for temporal prediction. We also demonstrated that the temporal derivative of the perceptual index tau (tau-dot) held predictive value for making collision judgements and varied inversely with activity in primary visual cortex (V1). Specifically, V1 activity increased with the increasing likelihood of reporting a collision, suggesting top-down attentional modulation of early visual processing areas as a function of subjective collision. Finally, egocentric viewpoints provoked a response bias for reporting collisions, rather than no-collisions, reflecting increased caution for head-on approaches. Associated increases in SMA activity suggest motor preparation mechanisms were engaged, despite the perceptual nature of the task.

Spatial relational learning and memory abilities do not differ between men and women in a real-world, open-field environment

This study assesses gender differences in spatial and non-spatial relational learning and memory in adult humans behaving freely in a real-world, open-field environment. In Experiment 1, we tested the use of proximal landmarks as conditional cues allowing subjects to predict the location of rewards hidden in one of two sets of three distinct locations. Subjects were tested in two different conditions: (1) when local visual cues marked the potentially-rewarded locations, and (2) when no local visual cues marked the potentially-rewarded locations. We found that only 17 of 20 adults (8 males, 9 females) used the proximal landmarks to predict the locations of the rewards. Although females exhibited higher exploratory behavior at the beginning of testing, males and females discriminated the potentially-rewarded locations similarly when local visual cues were present. Interestingly, when the spatial and local information conflicted in predicting the reward locations, males considered both spatial and local information, whereas females ignored the spatial information. However, in the absence of local visual cues females discriminated the potentially-rewarded locations as well as males. In Experiment 2, subjects (9 males, 9 females) were tested with three asymmetrically-arranged rewarded locations, which were marked by local cues on alternate trials. Again, females discriminated the rewarded locations as well as males in the presence or absence of local cues. In sum, although particular aspects of task performance might differ between genders, we found no evidence that women have poorer allocentric spatial relational learning and memory abilities than men in a real-world, open-field environment.

Les habiletés spatio-cognitives des aveugles de naissance : résolution de labyrinthes tactiles

La navigation repose en majeure partie sur la vision puisque ce sens nous permet de rassembler des informations spatiales de façon simultanée et de mettre à jour notre position par rapport à notre environnement. Pour plusieurs aveugles qui se fient à l’audition, le toucher, la proprioception, l’odorat et l’écholocation pour naviguer, sortir à l’extérieur de chez soi peut représenter un défi considérable. Les recherches sur le circuit neuronal de la navigation chez cette population en particulier s’avèrent donc primordiales pour mieux adapter les ressources aux handicapés visuels et réussir à les sortir de leur isolement. Les aveugles de naissance constituent aussi une population d’intérêt pour l’étude de la neuroplasticité. Comme leur cerveau s’est construit en absence d’intrant visuel, la plupart des structures reliées au sens de la vue sont réduites en volume par rapport à ceux de sujets voyants. De plus, leur cortex occipital, une région normalement dédiée à la vision, possède une activité supramétabolique au repos, ce qui peut représenter un territoire vierge pouvant être recruté par les autres modalités pour exécuter diverses tâches sensorielles. Plusieurs chercheurs ont déjà démontré l’implication de cette région dans des tâches sensorielles comme la discrimination tactile et la localisation auditive. D’autres changements plastiques de nature intramodale ont aussi été observés dans le circuit neuronal de la navigation chez ces aveugles. Par exemple, la partie postérieure de l’hippocampe, impliquée dans l’utilisation de cartes mentales, est réduite en volume alors que la section antérieure est élargie chez ces sujets. Bien que ces changements plastiques anatomiques aient bel et bien été observés chez les aveugles de naissance, il reste toutefois à les relier avec leur aspect fonctionnel. Le but de la présente étude était d’investiguer les corrélats neuronaux de la navigation chez l’aveugle de naissance tout en les reliant avec leurs habiletés spatio-cognitives. La première étude comportementale a permis d’identifier chez les aveugles congénitaux une difficulté d’apprentissage de routes tactiles construites dans des labyrinthes de petite échelle. La seconde étude, employant la technique d’imagerie par résonance magnétique fonctionnelle, a relié ces faiblesses au recrutement de régions cérébrales impliquées dans le traitement d’une perspective égocentrique, comme le lobule pariétal supérieur droit. Alors que des sujets voyants aux yeux bandés excellaient dans la tâche des labyrinthes, ces derniers recrutaient des structures impliquées dans un traitement allocentrique, comme l’hippocampe et le parahippocampe. Par ailleurs, la deuxième étude a confirmé le recrutement du cortex occipital dans une tâche de navigation chez les aveugles seulement. Ceci confirme l’implication de la plasticité intermodale dans des tâches cognitives de plus haut niveau, comme la navigation.

Learning associations between places and visual cues without learning to navigate: neither fornix nor entorhinal cortex is required

Rats with fornix transection, or with cytotoxic retrohippocampal lesions that removed entorhinal cortex plus ventral subiculum, performed a task that permits incidental learning about either allocentric (Allo) or egocentric (Ego) spatial cues without the need to navigate by them. Rats learned eight visual discriminations among computer-displayed scenes in a Y-maze, using the constant-negative paradigm. Every discrimination problem included two familiar scenes (constants) and many less familiar scenes (variables). On each trial, the rats chose between a constant and a variable scene, with the choice of the variable rewarded. In six problems, the two constant scenes had correlated spatial properties, either Alto (each constant appeared always in the same maze arm) or Ego (each constant always appeared in a fixed direction from the start arm) or both (Allo + Ego). In two No-Cue (NC) problems, the two constants appeared in randomly determined arms and directions. Intact rats learn problems with an added Allo or Ego cue faster than NC problems; this facilitation provides indirect evidence that they learn the associations between scenes and spatial cues, even though that is not required for problem solution. Fornix and retrohippocampal-lesioned groups learned NC problems at a similar rate to sham-operated controls and showed as much facilitation of learning by added spatial cues as did the controls; therefore, both lesion groups must have encoded the spatial cues and have incidentally learned their associations with particular constant scenes. Similar facilitation was seen in subgroups that had short or long prior experience with the apparatus and task. Therefore, neither major hippocampal input-output system is crucial for learning about allocentric or egocentric cues in this paradigm, which does not require rats to control their choices or navigation directly by spatial cues.

Gymnasts and orienteers display better mental rotation performance than nonathletes

The aim of this study was to examine whether athletes differ from nonathletes regarding their mental rotation performance. Furthermore, it investigated whether athletes doing sports requiring distinguishable levels of mental rotation (orienteering, gymnastics, running), as well as varying with respect to having an egocentric (gymnastics) or an allocentric perspective (orienteering), differ from each other. Therefore, the Mental Rotations Test (MRT) was carried out with 20 orienteers, 20 gymnasts, 20 runners, and 20 nonathletes. The results indicate large differences in mental rotation performance, with those actively doing sports outperforming the nonathletes. Analyses for the specific groups showed that orienteers and gymnasts differed from the nonathletes, whereas endurance runners did not. Contrary to expectations, the mental rotation performance of gymnasts did not differ from that of orienteers. This study also revealed gender differences in favor of men. Implications regarding a differentiated view of the connection between specific sports and mental rotation performance are discussed.

Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro

We investigated whether juvenile freshwater stingrays (Potamotrygon motoro) can solve spatial tasks by constructing a cognitive map of their environment. Two experimental conditions were run: allocentric and ego-allocentric. Rays were trained to locate food within a four-arm maze placed in a room with visual spatial cues. The feeding location (goal) within the maze (room) remained constant while the starting position varied for the allocentrically but not for the ego-allocentrically trained group. After training, all rays solved the experimental tasks; however, different orientation strategies were used within and between groups. Allocentrically trained rays reached the goal via novel routes starting from unfamiliar locations, while ego-allocentrically trained rays primarily solved the task on the basis of an egocentric turn response. Our data suggest that P. motoro orients by constructing a visual cognitive map of its environment, but also uses egocentric and/or other orientation strategies alone or in combination for spatial orientation, a choice which may be governed by the complexity of the problem. We conclude that spatial memory functions are a general feature of the vertebrate brain.