Navigational place learning in children and young adults as assessed with a standardized locomotor search task

Spatial behaviour was investigated using a spatial learning task based on the Radial Arm Maze, the Morris Water Maze, and open‐field search‐task procedures. Ninety‐six healthy children from six age groups (3, 4, 5, 7, 10 and 12 years) with no history of CNS disorders were studied with respect to the emergence of position‐, cue‐ and place responses. Participants were to detect x out of n hidden locations, frames of reference could be varied systematically, and three spatial memory errors and speed of navigation were recorded automatically. Task difficulties were equivalent for each age group. Results showed that navigational place learning was fully developed by the age of 10, whereas participants relied on cue orientation up to age 7. Even in the youngest group, the task could be achieved without relying on egocentric orientation, provided that proximal cues were presented. Most of the errors were of the reference memory type, whereas working memory errors were extremely rare. Speed of navigation markedly improved between age 5 and 7. An additional experiment showed that navigational place‐learning behaviour was clearly dependent on distal cues. A third study showed that in young adults, learning of the spatial layout improved, but performance on the place task did not improve any further. No sex differences were observed.     

Egocentric and allocentric navigation strategies in Williams syndrome and typical development

Recent findings suggest that difficulties on small‐scale visuospatial tasks documented in Williams syndrome (WS) also extend to large‐scale space. In particular, individuals with WS often present with difficulties in allocentric spatial coding (encoding relationships between items within an environment or array). This study examined the effect of atypical spatial processing in WS on large‐scale navigational strategies, using a novel 3D virtual environment. During navigation of recently learnt large‐scale space, typically developing (TD) children predominantly rely on the use of a sequential egocentric strategy (recalling the sequence of left–right body turns throughout a route), but become more able to use an allocentric strategy between 5 and 10 years of age. The navigation strategies spontaneously employed by TD children between 5 and 10 years of age and individuals with WS were analysed. The ability to use an allocentric strategy on trials where spatial relational knowledge was required to find the shortest route was also examined. Results showed that, unlike TD children, during spontaneous navigation the WS group did not predominantly employ a sequential egocentric strategy. Instead, individuals with WS followed the path until the correct environmental landmarks were found, suggesting the use of a time‐consuming and inefficient view‐matching strategy for wayfinding. Individuals with WS also presented with deficits in allocentric spatial coding, demonstrated by difficulties in determining short‐cuts when required and difficulties developing a mental representation of the environment layout. This was found even following extensive experience in an environment, suggesting that – unlike in typical development – experience cannot contribute to the development of spatial relational processing in WS. This atypical presentation of both egocentric and allocentric spatial encoding is discussed in relation to specific difficulties on small‐scale spatial tasks and known atypical cortical development in WS.     

Underlying Spatial Skills to Support Navigation Through Large,Unconstrained Environments

Studies of spatial navigation in real‐world settings have been limited to neighborhoods, campuses, and buildings. These locations have structural components, such as roads or hallways, which may direct navigation. The current study assessed navigational skills within a large‐scale forested environment that contained few pre‐established paths. Participants were asked to find flags using only a map and compass; dependent variables included target‐finding accuracy and efficiency. In addition, measurements of sense of direction, strategy, and working memory were taken to identify how these cognitive abilities influence performance. The results demonstrate the expected correlations between sense of direction and navigational success. An unexpected correlation between spatial working memory and navigational success was also found, which was the only significant predictor of performance when all measures were regressed together. These results suggest that studies should not forget basic cognitive abilities, which may predict success more than measures of sense of direction. Copyright © 2015 John Wiley & Sons, Ltd.     

Age-related similarities and differences in monitoring spatial cognition

Spatial cognitive performance is impaired in later adulthood but it is unclear whether the metacognitive processes involved in monitoring spatial cognitive performance are also compromised. Inaccurate monitoring could affect whether people choose to engage in tasks that require spatial thinking and also the strategies they use in spatial domains such as navigation. The current experiment examined potential age differences in monitoring spatial cognitive performance in a variety of spatial domains including visual–spatial working memory, spatial orientation, spatial visualization, navigation, and place learning. Younger and older adults completed a 2D mental rotation test, 3D mental rotation test, paper folding test, spatial memory span test, two virtual navigation tasks, and a cognitive mapping test. Participants also made metacognitive judgments of performance (confidence judgments, judgments of learning, or navigation time estimates) on each trial for all spatial tasks. Preference for allocentric or egocentric navigation strategies was also measured. Overall, performance was poorer and confidence in performance was lower for older adults than younger adults. In most spatial domains, the absolute and relative accuracy of metacognitive judgments was equivalent for both age groups. However, age differences in monitoring accuracy (specifically relative accuracy) emerged in spatial tasks involving navigation. Confidence in navigating for a target location also mediated age differences in allocentric navigation strategy use. These findings suggest that with the possible exception of navigation monitoring, spatial cognition may be spared from age-related decline even though spatial cognition itself is impaired in older age.     

Introducing a new age-and-cognition-sensitive measurement for assessing spatial orientation using a landmark-less virtual reality navigational task

Age-related impairments during spatial navigation have been widely reported in egocentric and allocentric paradigms. However, the effect of age on more specific navigational components such as the ability to drive or update directional information has not received enough attention. In this study we investigated the effect of age on spatial updating of a visual target after a series of whole–body rotations and transitions using a novel landmark-less virtual reality (VR) environment. Moreover, a significant number of previous studies focused on measures susceptible to a general decline in motor skills such as the spent time navigating, the distance traversed. The current paper proposes a new compound spatial measure to assess navigational performance, examines its reliability and compares its power with those of the measures of duration and traversed distance in predicting participants' age and cognitive groups assessed by Montreal Cognitive Assessment (MoCA) scores. Using data from 319 adults (20–83 years), our results confirm the reliability, the age sensitivity, and the cognitive validity of the designed spatial measure as well as its superiority to the measures of duration and traversed distance in predicting age and MoCA score. In addition, the results show the significant effect of age cognitive status on spatial updating.     

Developmental differences in memory for cross‐modal associations

Associative learning is critical to normal cognitive development in children. However, young adults typically outperform children on paired‐associate tasks involving visual, verbal and spatial location stimuli. The present experiment investigated cross‐modal odour–place associative memory in children (7–10 years) and young adults (18–24 years). During the study phase, six odours were individually presented and paired with one of 12 spatial locations on a board. During the test phase, participants were presented with the six stimuli individually and were asked to place each stimulus on the correct spatial location. Children committed significantly more errors on the odour–place task than did young adults. However, item recognition memory for the odours or spatial locations involved in the odour–place associative memory task was similar between children and young adults. Therefore, poor odour–place associative memory in children did not result from impaired memory for the individual odours or spatial locations involved in the associations. The results suggest that cross‐modal associative memory is not fully developed in children.     

Development of allocentric spatial recall from new viewpoints in virtual reality

Using landmarks and other scene features to recall locations from new viewpoints is a critical skill in spatial cognition. In an immersive virtual reality task, we asked children 3.5–4.5 years old to remember the location of a target using various cues. On some trials they could use information from their own self‐motion. On some trials they could use a view match. In the very hardest kind of trial, they were ‘teleported’ to a new viewpoint and could only use an allocentric spatial representation. This approach provides a strict test for allocentric coding (without either a matching viewpoint or self‐motion information) while avoiding additional task demands in previous studies (it does not require them to deal with a small table‐top environment or to manage stronger cue conflicts). Both the younger and older groups were able to point back at the target location better than chance when they could use view matching and/or self‐motion, but allocentric recall was only seen in the older group (4.0–4.5). In addition, we only obtained evidence for a specific kind of allocentric recall in the older group: they tracked one major axis of the space significantly above chance, r(158) = .28, but not the other, r(158) = ?.01. We conclude that there is a major qualitative change in coding for spatial recall around the fourth birthday, potentially followed by further development towards fully flexible recall from new viewpoints.     

Dissociable spatial memory systems revealed by typical and atypical human development

Rodent lesion studies have revealed the existence of two causally dissociable spatial memory systems, localized to the hippocampus and striatum that are preferentially sensitive to environmental boundaries and landmark objects, respectively. Here we test whether these two memory systems are causally dissociable in humans by examining boundary‐ and landmark‐based memory in typical and atypical development. Adults with Williams syndrome (WS)—a developmental disorder with known hippocampal abnormalities—and typical children and adults, performed a navigation task that involved learning locations relative to a boundary or a landmark object. We found that boundary‐based memory was severely impaired in WS compared to typically‐developing mental‐age matched (MA) children and chronological‐age matched (CA) adults, whereas landmark‐based memory was similar in all groups. Furthermore, landmark‐based memory matured earlier in typical development than boundary‐based memory, consistent with the idea that the WS cognitive phenotype arises from developmental arrest of late maturing cognitive systems. Together, these findings provide causal and developmental evidence for dissociable spatial memory systems in humans.     

边界促进空间导航的认知神经机制

边界是指在人的视野中占据较大比例,且具有立体拓展平面的障碍物,对于人类和动物的空间导航行为具有极大的促进作用。认知发展研究发现儿童早期(1岁半～2岁)通过加工边界的空间几何结构实现物体定位,并且随着年龄的发展逐渐学会利用边界的高度信息(3.1岁～4.7岁)、长度信息(4～5岁)、视觉阻碍性信息(5岁)等完成空间导航。基于这些认知过程,神经影像学研究主要以成人为研究被试,发现大脑中的内侧颞叶和顶叶脑区在边界加工中有着不同功能作用。具体而言,边界的空间几何结构及构成要素(高度、长度和角度)体位置的学习和提取则由海马负责。但是,仍存在一些研究问题值得未来深入S探c讨i。e第n一c,e拓展深化边界促进与后顶叶之间的功能交互。第三,密切关注大脑对场地边界与场地中心编码的心理或神经表征的区别和联系。第四,重点考察阿尔兹海默症有关基因易感人群在基于边界导航的行为受损情况。最后,延伸探讨边界在长时记忆、时间知觉、视觉空间、社交网络等领域的影响机制。     

Evidence of separable spatial representations in a virtual navigation task

Three experiments investigated spatial orientation in a virtual navigation task. Subjects had to adjust a homing vector indicating their end position relative to the origin of the path. It was demonstrated that sparse visual flow was sufficient for accurate path integration. Moreover, subjects were found to prefer a distinct egocentric or allocentric reference frame to solve the task. "Turners" reacted as if they had taken on the new orientation during turns of the path by mentally rotating their sagittal axis (egocentric frame). "Nonturners," by contrast, tracked the new orientation without adopting it (allocentric frame). When instructed to use their nonpreferred reference frame, both groups displayed no decline in response accuracy relative to their preferred frame; even when presented with reaction formats based on either ego or allocentric coordinates, with format unpredictable on a trial, both groups responded highly accurately. These findings support the assumption of coexisting spatial representations during navigation.     

The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze

BackgroundPresent evidence suggests that the hippocampus (HC) and the parahippocampal cortex (PHC) are involved in allocentric (world-centered) spatial memory. However, the putative role of the PHC in egocentric (body-centered) spatial learning has received only limited systematic investigation.MethodsTo examine the role of the PHC in egocentric learning, 19 healthy volunteers learned to find their way in a virtual maze during functional magnetic resonance imaging (fMRI). The virtual maze presented a first-person view, lacked any topographical landmarks and could be learned only using egocentric navigation strategies.ResultsDuring learning, increased medial temporal lobe activity was observed in the PHC bilaterally. Activity was also observed in cortical areas known to project to the PHC and proposed to contribute to egocentric spatial navigation and memory.ConclusionsOur results point to a role of the PHC for the representation and storage of egocentric information. It seems possible that the PHC contributes to egocentric memory by its feedback projections to the posterior parietal cortex. Moreover, access to allocentric and egocentric streams of spatial information may enable the PHC to construct a global and comprehensive representation of spatial environments and to promote the construction of stable cognitive maps by translating between egocentric and allocentric frames of memory.     

Developmental time course of the acquisition of sequential egocentric and allocentric navigation strategies

Navigation in a complex environment can rely on the use of different spatial strategies. We have focused on the employment of “allocentric” (i.e., encoding interrelationships among environmental cues, movements, and the location of the goal) and “sequential egocentric” (i.e., sequences of body turns associated with specific choice points) strategies during navigation. To investigate the developmental pattern of these two strategies in school-aged children, we used a virtual reality paradigm in which the spontaneous or imposed use of both strategies could be assessed. Our results showed an increase in spontaneous use of the allocentric strategy and also an increase in reliance on environmental landmarks with age. Although a majority of the children spontaneously used the sequential egocentric strategy, all age groups performed above chance when the allocentric strategy was imposed. Altogether, our findings suggest that young children are able to employ an allocentric strategy but that the nature of this allocentric strategy changes progressively in a complex cognitive representation between 5 and 10 years of age.     

Using hippocampal‐dependent eyeblink conditioning to predict individual differences in spatial reorientation strategies in 3‐ to 6‐year‐olds

The hippocampus is a subcortical structure in the medial temporal lobe involved in cognitive functions such as spatial navigation and reorientation, episodic memory, and associative learning. While much is understood about the role of hippocampal function in learning and memory in adults, less is known about the relations between the hippocampus and the development of these cognitive skills in young children due to the limitations of using standard methods (e.g., MRI) to examine brain structure and function in developing populations. This study used hippocampal‐dependent trace eyeblink conditioning (EBC) as a feasible approach to examine individual differences in hippocampal functioning as they relate to spatial reorientation and episodic memory performance in young children. Three‐ to six‐year‐old children (N = 50) completed tasks that measured EBC, spatial reorientation, and episodic memory, as well as non‐hippocampal‐dependent processing speed abilities. Results revealed that when age was held constant, individual differences in EBC performance were significantly related to individual differences in performance on the spatial reorientation test, but not on the episodic memory or processing speed tests. When the relations between hippocampal‐dependent EBC and different reorientation strategies were explored, it was found that individual differences in hippocampal function predicted the use of geometric information for reorienting in space as opposed to a combined strategy that uses both geometric information and salient visual cues. The utilization of eyeblink conditioning to examine hippocampal function in young populations and its implications for understanding the dissociation between spatial reorientation and episodic memory development are discussed.     

Development of navigational working memory: Evidence from 6‐ to 10‐year‐old children

The ability to learn complex environments may require the contribution of different types of working memory. Therefore, we investigated the development of different types of working memory (navigational, reaching, and verbal) in 129 typically developing children. We aimed to determine whether navigational working memory develops at the same rate as other types of working memory and whether the gender differences reported in adults are already present during development. We found that navigational working memory is less developed than both verbal and reaching working memory and that gender predicts performance only for navigational working memory. Our results are in line with reports that children made significantly more errors in far space than adults, showing that near space representation develops before far space representation.     

Preserved learning about allocentric cues but impaired flexible memory expression in rats with hippocampal lesions

Several studies have shown that slight modifications in the standard reference spatial memory procedure normally used for allocentric learning in the Morris water maze and the radial maze, can overcome the classic deficit in allocentric navigation typically observed in rats with hippocampal damage. In these special paradigms, however, there is only intramaze manipulation of a salient stimulus. The present study was designed to investigate whether extramaze manipulations produce a similar outcome. With this aim a four-arm plus-shaped maze and a reference spatial memory paradigm were used, in which the goal arm was marked in two ways: by a prominent extramaze cue (intermittent light), which maintained a constant relation with the goal, and by the extramaze constellation of stimuli around the maze. Experiment 1 showed that, unlike the standard version of the task, using this special training procedure hippocampally-damaged rats could learn a place response as quickly as control animals; importantly, one day after reaching criterion, lesioned and control subjects performed the task perfectly during a transfer test in which the salient extramaze stimulus used during the acquisition was removed. However, although acquisition deficit was overcomed in these lesioned animals, a profound deficit in retention was detected 15 days later. Experiment 2 suggests that although under our special paradigm hippocampal rats can learn a place response, spatial memory only can be expressed when the requisites of behavioral flexibility are minimal. These findings suggest that, under certain circumstances, extrahippocampal structures are sufficient for building a coherent allocentric representation of space; however, flexible memory expression is dependent, fundamentally, on hippocampal functioning.     

Stepping Into a Map: Initial Heading Direction Influences Spatial Memory Flexibility

Learning a novel environment involves integrating first‐person perceptual and motoric experiences with developing knowledge about the overall structure of the surroundings. The present experiments provide insights into the parallel development of these egocentric and allocentric memories by intentionally conflicting body‐ and world‐centered frames of reference during learning, and measuring outcomes via online and offline measures. Results of two experiments demonstrate faster learning and increased memory flexibility following route perspective reading (Experiment 1) and virtual navigation (Experiment 2) when participants begin exploring the environment on a northward (vs. any other direction) allocentric heading. We suggest that learning advantages due to aligning body‐centered (left/right/forward/back) with world‐centered (NSEW) reference frames are indicative of three features of spatial memory development and representation. First, memories for egocentric and allocentric information develop in parallel during novel environment learning. Second, cognitive maps have a preferred orientation relative to world‐centered coordinates. Finally, this preferred orientation corresponds to traditional orientation of physical maps (i.e., north is upward), suggesting strong associations between daily perceptual and motor experiences and the manner in which we preferentially represent spatial knowledge.     

Development of egocentric and allocentric spatial representations from childhood to elderly age

Spatial reference frames are fundamental to represent the position of objects or places. Although research has reported changes in spatial memory abilities during childhood and elderly age, no study has assessed reference frames processing during the entire lifespan using the same task. Here, we aimed at providing some preliminary data on the capacity to process reference frames in 283 healthy participants from 6 to 89 years of age. A spatial memory task requiring egocentric/allocentric verbal judgments about objects in peri-/extrapersonal space was used. The main goals were: (1) tracing a baseline of the normal process of development of these spatial components; (2) clarifying if reference frames are differently vulnerable to age-related effects. Results showed a symmetry between children of 6–7 years and older people of 80–89 years who were slower and less accurate than all other age groups. As regards processing time, age had a strong effect on the allocentric component, especially in extrapersonal space, with a longer time in 6- to 7-year-old children and 80- to 89-year-old adults. The egocentric component looked less affected by aging. Regarding the level of spatial ability (accuracy), the allocentric ability appeared less sensitive to age-related variations, whereas the egocentric ability progressively improved from 8 years and declined from 60 years. The symmetry in processing time and level of spatial ability is discussed in relation to the development of executive functions and to the structural and functional changes due to incomplete maturation (in youngest children) and deterioration (in oldest adults) of underlying cerebral areas.     

Egocentric metric representations in peripersonal space: A bridge between motor resources and spatial memory

Research on visuospatial memory has shown that egocentric (subject-to-object) and allocentric (object-to-object) reference frames are connected to categorical (non-metric) and coordinate (metric) spatial relations, and that motor resources are recruited especially when processing spatial information in peripersonal (within arm reaching) than extrapersonal (outside arm reaching) space. In order to perform our daily-life activities, these spatial components cooperate along a continuum from recognition-related (e.g., recognizing stimuli) to action-related (e.g., reaching stimuli) purposes. Therefore, it is possible that some types of spatial representations rely more on action/motor processes than others. Here, we explored the role of motor resources in the combinations of these visuospatial memory components. A motor interference paradigm was adopted in which participants had their arms bent behind their back or free during a spatial memory task. This task consisted in memorizing triads of objects and then verbally judging what was the object: (1) closest to/farthest from the participant (egocentric coordinate); (2) to the right/left of the participant (egocentric categorical); (3) closest to/farthest from a target object (allocentric coordinate); and (4) on the right/left of a target object (allocentric categorical). The triads appeared in participants' peripersonal (Experiment 1) or extrapersonal (Experiment 2) space. The results of Experiment 1 showed that motor interference selectively damaged egocentric-coordinate judgements but not the other spatial combinations. The results of Experiment 2 showed that the interference effect disappeared when the objects were in the extrapersonal space. A third follow-up study using a within-subject design confirmed the overall pattern of results. Our findings provide evidence that motor resources play an important role in the combination of coordinate spatial relations and egocentric representations in peripersonal space.     

Age and active navigation effects on episodic memory: A virtual reality study

We investigated the navigation‐related age effects on learning, proactive interference semantic clustering, recognition hits, and false recognitions in a naturalistic situation using a virtual apartment‐based task. We also examined the neuropsychological correlates (executive functioning [EF] and episodic memory) of navigation‐related age effects on memory. Younger and older adults either actively navigated or passively followed the computer‐guided tour of an apartment. The results indicated that active navigation increased recognition hits compared with passive navigation, but it did not influence other memory measures (learning, proactive interference, and semantic clustering) to a similar extent in either age group. Furthermore, active navigation helped to reduce false recognitions in younger adults but increased those made by older adults. This differential effect of active navigation for younger and older adults was accounted for by EF score. Like for the subject‐performed task effects, the effects from the navigation manipulation were well accounted for by item‐specific/relational processing distinction, and they were also consistent with a source monitoring deficit in older adults.     

Persistent and stable biases in spatial learning mechanisms predict navigational style

A wealth of evidence in rodents and humans supports the central roles of two learning systems—hippocampal place learning and striatal response learning—in the formation of spatial representations to support navigation. Individual differences in the ways that these mechanisms are engaged during initial encoding and subsequent navigation may provide a powerful framework for explaining the wide range of variability found in the strategies and solutions that make up human navigational styles. Previous work has revealed that activation in the hippocampal and striatal networks during learning could predict navigational style. Here, we used functional magnetic resonance imaging to investigate the relative activations in these systems during both initial encoding and the act of dynamic navigation in a learned environment. Participants learned a virtual environment and were tested on subsequent navigation to targets within the environment. We observed that a given individual had a consistent balance of memory system engagement across both initial encoding and subsequent navigation, a balance that successfully predicted the participants’ tendencies to use novel shortcuts versus familiar paths during dynamic navigation. This was further supported by the observation that the activation during subsequent retrieval was not dependent on the type of solution used on a given trial. Taken together, our results suggest a model in which the place- and response-learning systems are present in parallel to support a variety of navigational behaviors, but stable biases in the engagement of these systems influence what solutions might be available for any given individual.