Age-related effects on spatial memory across viewpoint changes relative to different reference frames

Remembering object positions across different views is a fundamental competence for acting and moving appropriately in a large-scale space. Behavioural and neurological changes in elderly subjects suggest that the spatial representations of the environment might decline compared to young participants. However, no data are available on the use of different reference frames within topographical space in aging. Here we investigated the use of allocentric and egocentric frames in aging, by asking young and older participants to encode the location of a target in a virtual room relative either to stable features of the room (allocentric environment-based frame), or to an unstable objects set (allocentric objects-based frame), or to the viewer's viewpoint (egocentric frame). After a viewpoint change of 0$,^{circ}$ (absent), 45$,^{circ}$ (small) or 135$,^{circ}$ (large), participants judged whether the target was in the same spatial position as before relative to one of the three frames. Results revealed a different susceptibility to viewpoint changes in older than young participants. Importantly, we detected a worst performance, in terms of reaction times, for older than young participants in the allocentric frames. The deficit was more marked for the environment-based frame, for which a lower sensitivity was revealed as well as a worst performance even when no viewpoint change occurred. Our data provide new evidence of a greater vulnerability of the allocentric, in particular environment-based, spatial coding with aging, in line with the retrogenesis theory according to which cognitive changes in aging reverse the sequence of acquisition in mental development

Differential recruitment of brain networks following route and cartographic map learning of spatial environments.

An extensive neuroimaging literature has helped characterize the brain regions involved in navigating a spatial environment. Far less is known, however, about the brain networks involved when learning a spatial layout from a cartographic map. To compare the two means of acquiring a spatial representation, participants learned spatial environments either by directly navigating them or learning them from an aerial-view map. While undergoing functional magnetic resonance imaging (fMRI), participants then performed two different tasks to assess knowledge of the spatial environment: a scene and orientation dependent perceptual (SOP) pointing task and a judgment of relative direction (JRD) of landmarks pointing task. We found three brain regions showing significant effects of route vs. map learning during the two tasks. Parahippocampal and retrosplenial cortex showed greater activation following route compared to map learning during the JRD but not SOP task while inferior frontal gyrus showed greater activation following map compared to route learning during the SOP but not JRD task. We interpret our results to suggest that parahippocampal and retrosplenial cortex were involved in translating scene and orientation dependent coordinate information acquired during route learning to a landmark-referenced representation while inferior frontal gyrus played a role in converting primarily landmark-referenced coordinates acquired during map learning to a scene and orientation dependent coordinate system. Together, our results provide novel insight into the different brain networks underlying spatial representations formed during navigation vs. cartographic map learning and provide additional constraints on theoretical models of the neural basis of human spatial representation

Lost in spatial translation - A novel tool to objectively assess spatial disorientation in Alzheimer's disease and frontotemporal dementia

Spatial disorientation is a prominent feature of early Alzheimer's disease (AD) attributed to degeneration of medial temporal and parietal brain regions, including the retrosplenial cortex (RSC). By contrast, frontotemporal dementia (FTD) syndromes show generally intact spatial orientation at presentation. However, currently no clinical tasks are routinely administered to objectively assess spatial orientation in these neurodegenerative conditions. In this study we investigated spatial orientation in 58 dementia patients and 23 healthy controls using a novel virtual supermarket task as well as voxel-based morphometry (VBM). We compared performance on this task with visual and verbal memory function, which has traditionally been used to discriminate between AD and FTD. Participants viewed a series of videos from a first person perspective travelling through a virtual supermarket and were required to maintain orientation to a starting location. Analyses revealed significantly impaired spatial orientation in AD, compared to FTD patient groups. Spatial orientation performance was found to discriminate AD and FTD patient groups to a very high degree at presentation. More importantly, integrity of the RSC was identified as a key neural correlate of orientation performance. These findings confirm the notion that i) it is feasible to assess spatial orientation objectively via our novel Supermarket task; ii) impaired orientation is a prominent feature that can be applied clinically to discriminate between AD and FTD and iii) the RSC emerges as a critical biomarker to assess spatial orientation deficits in these neurodegenerative conditions

Enhancing allocentric spatial recall in pre-schoolers through navigational training programme

Unlike for other abilities, children do not receive systematic spatial orientation training at school, even though navigational training during adulthood improves spatial skills. We investigated whether navigational training programme (NTP) improved spatial orientation skills in pre-schoolers. We administered 12-week NTP to seventeen 4- to 5-year-old children (training group, TG). The TG children and 17 age-matched children (control group, CG) who underwent standard didactics were tested twice before (T0) and after (T1) the NTP using tasks that tap into landmark, route and survey representations. We determined that the TG participants significantly improved their performances in the most demanding navigational task, which is the task that taps into survey representation. This improvement was significantly higher than that observed in the CG, suggesting that NTP fostered the acquisition of survey representation. Such representation is typically achieved by age seven. This finding suggests that NTP improves performance on higher-level navigational tasks in pre-schooler

Virtual enactment effect on memory in young and aged populations: a systematic review

Background: Spatial cognition is a critical aspect of episodic memory, as it provides the scaffold for events and enables successful retrieval. Virtual enactment (sensorimotor and cognitive interaction) by means of input devices within virtual environments provides an excellent opportunity to enhance encoding and to support memory retrieval with useful traces in the brain compared to passive observation. Methods: We conducted a systematic review with Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines concerning the virtual enactment effect on spatial and episodic memory in young and aged populations. We aim at giving guidelines for virtual enactment studies, especially in the context of aging, where spatial and episodic memory decline. Results: Our findings reveal a positive effect on spatial and episodic memory in the young population and promising outcomes in aging. Several cognitive factors (e.g., executive function, decision-making, and visual components) mediate memory performances. Findings should be taken into account for future interventions in aging. Conclusions: The present review sheds light on the key role of the sensorimotor and cognitive systems for memory rehabilitation by means of a more ecological tool such as virtual reality and stresses the importance of the body for cognition, endorsing the view of an embodied mind

Challenges for identifying the neural mechanisms that support spatial navigation: the impact of spatial scale.

Spatial navigation is a fascinating behavior that is essential for our everyday lives. It involves nearly all sensory systems, it requires numerous parallel computations, and it engages multiple memory systems. One of the key problems in this field pertains to the question of reference frames: spatial information such as direction or distance can be coded egocentrically-relative to an observer-or allocentrically-in a reference frame independent of the observer. While many studies have associated striatal and parietal circuits with egocentric coding and entorhinal/hippocampal circuits with allocentric coding, this strict dissociation is not in line with a growing body of experimental data. In this review, we discuss some of the problems that can arise when studying the neural mechanisms that are presumed to support different spatial reference frames. We argue that the scale of space in which a navigation task takes place plays a crucial role in determining the processes that are being recruited. This has important implications, particularly for the inferences that can be made from animal studies in small scale space about the neural mechanisms supporting human spatial navigation in large (environmental) spaces. Furthermore, we argue that many of the commonly used tasks to study spatial navigation and the underlying neuronal mechanisms involve different types of reference frames, which can complicate the interpretation of neurophysiological data

Egocentric and allocentric spatial reference frames in aging: A systematic review

Abstract 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)

Maladaptive bias for extrahippocampal navigation strategies in aging humans.

Efficient spatial navigation requires not only accurate spatial knowledge but also the selection of appropriate strategies. Using a novel paradigm that allowed us to distinguish between beacon, associative cue, and place strategies, we investigated the effects of cognitive aging on the selection and adoption of navigation strategies in humans. Participants were required to rejoin a previously learned route encountered from an unfamiliar direction. Successful performance required the use of an allocentric place strategy, which was increasingly observed in young participants over six experimental sessions. In contrast, older participants, who were able to recall the route when approaching intersections from the same direction as during encoding, failed to use the correct place strategy when approaching intersections from novel directions. Instead, they continuously used a beacon strategy and showed no evidence of changing their behavior across the six sessions. Given that this bias was already apparent in the first experimental session, the inability to adopt the correct place strategy is not related to an inability to switch from a firmly established response strategy to an allocentric place strategy. Rather, and in line with previous research, age-related deficits in allocentric processing result in shifts in preferred navigation strategies and an overall bias for response strategies. The specific preference for a beacon strategy is discussed in the context of a possible dissociation between beacon-based and associative-cue-based response learning in the striatum, with the latter being more sensitive to age-related changes

Decision in space

Human navigation is generally believed to rely on two types of strategy adoption, route- based and map-based strategies. Both types of navigation require making spatial decisions along the traversed way. Nevertheless, formal computational and neural links between navigational strategies and mechanisms of value based decision making have so far been underexplored in humans. Here, we employed functional magnetic resonance imaging (fMRI) while subjects located different target objects in a virtual environment. We then modelled their paths using reinforcement learning (RL) algorithms, which successfully explain decision behaviour and its neural correlates. Our results show that subjects used a mixture of route and map-based navigation, and their paths could be well explained by the model-free and model-based RL algorithms. Furthermore, the value signals of model-free choices during route-based navigation modulated the BOLD signals in the ventro-medial prefrontal cortex (vmPFC). On the contrary, the BOLD signals in parahippocampal and medial temporal lobe (MTL) regions pertained to model- based value signals during map-based navigation. Our findings suggest that the brain might share computational mechanisms and neural substrates for navigation and value- based decisions, such that model-free choice guides route-based navigation and model- based choice directs map-based navigation. These findings open new avenues for computational modelling of wayfinding by directing attention to value-based decision, differing from common direction and distances approaches. The ability to find one’s way in a complex environment is crucial to everyday functioning. This navigational ability relies on the integrity of several cognitive functions and different strategies, route and map-based navigation, that individuals may adopt while navigating in the environment. As the integrity of these cognitive functions often decline with age, navigational abilities show marked changes in both normal aging and dementia. Combining a wayfinding task in a virtual reality (VR) environment and modeling technique based on reinforcement learning (RL) algorithms, we investigated the effects of cognitive aging on the selection and adoption of navigation strategies in human. The older participants performed the wayfinding task while undergoing functional Magnetic Resonance Imaging (fMRI), and the younger participants performed the same task outside the MRI machine. Compared with younger participants, older participants traversed a longer distance. They also exhibited a higher tendency to repeat previously established routes to locate the target objects. Despite these differences, the traversed paths in both groups could be well explained by the model-free and model-based RL algorithms. Furthermore, neuroimaging results from the older participants show that BOLD signal in the ventromedial prefrontal cortex (vmPFC) pertained to model-free value signals. This result provide evidence on the utility of the RL algorithms to explain how the aging brain computationally prefer to rely more on the route-based navigation