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

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Abstract

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.

Introduction

Within spatial memory, a traditional distinction has been made between “allocentric” (world-centered) and “egocentric” (body-centered) representations (Arleo and Rondi-Reig, 2007, Burgess, 2006, Burgess, 2008). In rodents, allocentric (or place-learning) navigation is shown to depend on the hippocampus, whereas simple egocentric (stimulus–response like) navigation depends on the dorsal striatum (Morris et al., 1982, O’Keefe and Nadel, 1978, Packard and Knowlton, 2002, White and McDonald, 2002). In more complex tasks, the hippocampus has been shown to be involved in not only allocentric (Aggleton and Brown, 1999, Burgess et al., 2002, Byrne et al., 2007, O’Keefe and Nadel, 1978) but also in associative (Diana, Yonelinas, & Ranganath, 2007), sequential (Morris, 2001), or flexible (Eichenbaum, 2004, Rondi-Reig et al., 2001) relational representations. Moreover, Rondi-Reig and colleagues (2006) showed that an additional “sequential egocentric” representation is dependent on the rodent hippocampus. A sequential egocentric strategy refers to the memorization of temporal relations between specific environmental choice points. The sequential egocentric strategy differs from a dead reckoning process in the sense that it does not allow online localization but rather allows the memory of temporal order of body turns associated with spatially distinct choice points.

The hippocampus in adult humans has likewise been associated with allocentric representations of location, allowing accurate navigation from new starting locations (Hartley, Trinkler, & Burgess, 2004) based on the configuration of environmental cues (Doeller and Burgess, 2008, Iaria et al., 2003) or recognition of locations from a new viewpoint (Abrahams et al., 1997, King et al., 2002, Lambrey et al., 2008). Navigation via a fixed route (Hartley et al., 2004, Iaria et al., 2003) or relative to a single landmark (Doeller & Burgess, 2008), consistent with simple egocentric representations, has been associated with the dorsal striatum. In line with the findings of Rondi-Reig and colleagues (2006), it recently has been shown that the hippocampus is involved in human navigation when the egocentric reference frame used involves temporal sequential ordering such as during the sequential egocentric strategy (Iglói, Doeller, Berthoz, Rondi-Reig, & Burgess, 2010).

In the current study, we were specifically interested in the developmental time course of the sequential egocentric and allocentric representations in children. Children of different ages were tested on a task in which they either were free to spontaneously use one strategy or the other or were “forced” to use the allocentric strategy. Early developmental work on spatial abilities suggested a shift from the use of egocentric representations to allocentric ones with age (Acredolo, 1978, Bremner and Bryant, 1977); in several training trials, 6- to 16-month-olds learned to locate an object on one side of their body midline and, after being turned around, were motivated to find back the object from the opposite side of the room or table. The 9- to 11-month-olds responded in an egocentric way, searching for the object on their body side where they had found it before, whereas the 16-month-olds searched for the object in the correct location in space. In addition, early empirical studies (Huttenlocher and Presson, 1973, Piaget and Inhelder, 1948) observed that allocentric representations develop well into the school years. Perspective-taking studies (e.g., the well-known “three mountain task” of Piaget & Inhelder, 1948) showed that until 9 or 10 years of age, children make a high rate of egocentric errors, suggesting their great reliance on this memory system. Similarly, it was shown that children younger than 5 years do not perform as well as older children and adults on keeping track of where they are in an eight-arm radial maze (Aadland et al., 1985, Foreman et al., 1984). Also, experiments testing children in a Morris maze paradigm showed that place learning develops up to 7 to 10 years of age (Overman et al., 1996, Lehnung et al., 1998, Leplow et al., 2003). However, allocentric representations appear to be present in younger children; accurate representations of locations within a testing room have been shown already at 36 months of age (Nardini et al., 2006, Newcombe et al., 1998), and children as young as 5 years are able to use a nonegocentric strategy if local landmarks are provided (Bullens et al., 2010, Lehnung et al., 1998). Therefore, converging evidence seems to indicate a gradual acquisition of the ability to use allocentric representations with age. It has been proposed that this developmental pattern is related to the delayed maturation of the hippocampus (Newcombe and Huttenlocher, 2003, Newcombe and Learmonth, 1999, Overman et al., 1996). Recently, it has been suggested that part of the difficulties young children have with complex goal-oriented tasks might be explained by their inability to correctly integrate multiple (i.e., visual and proprioceptive) sources of information (Nardini, Jones, Bedford, & Braddick, 2008).

Although the above-described studies did provide insight into the development of egocentric and allocentric representations, they did not assess complex navigation strategies in children involving movement over time and complex goal-oriented behavior. Interestingly, it has been suggested that the use of an allocentric strategy emerges when children acquire movement and walking skills (Newcombe & Learmonth, 1999). It is striking that although considerable improvement in navigation is observed over the school years, much remains unknown about when specific navigation strategies (i.e., egocentric and allocentric) appear in children. In the current study, we investigated the spontaneous use of navigation strategies in children of different ages in a dynamic goal-directed paradigm. Here 5-, 7-, and 10-year-olds were tested on the virtual reality adaptation of the StarMaze task (Iglói, Zaoui, Berthoz, & Rondi-Reig, 2009) previously used to assess navigation strategies in rodents (Rondi-Reig et al., 2006). The use of virtual environments has proved to be a good and reliable tool for studying spatial cognition in general (Péruch & Wilson, 2004) and in studying developmental patterns in spatial knowledge more specifically (Schmelter, Jansen, & Heil, 2009). The virtual StarMaze task consisted of a pentagonal maze with five radiating arms in which participants navigated to a goal. Two tasks were performed: a multiple strategies task and an allocentric task. In the multiple strategies task, it could be examined whether and in which phase(s) of the learning process children spontaneously used a sequential egocentric navigation strategy or an allocentric one to locate the goal. The allocentric task specifically characterized the nature of the allocentric strategy children used. Based on the developmental literature described above, we expected all age groups to preferably use an egocentric navigation strategy. Furthermore, we anticipated finding a gradual acquisition of the ability to use an allocentric strategy that, in addition, might change in nature with age. This study extends previous findings showing that all age groups were able to use an allocentric strategy and that the egocentric strategy was not abandoned with age.

Section snippets

Participants

A total of 77 children from 5 to 10 years of age were recruited from an elementary school situated in The Netherlands to participate in the study. In the group of 5-year-olds, only those children who learned the training route themselves (n = 7) or who, after the third trial, were shown the correct route by the experimenter and thereafter learned the route in a maximum of two trials (n = 10) were included. A total of 20 children (16 5-year-olds, 2 7-year-olds, and 2 10-year-olds) were excluded from

Results

In the multiple strategies task, it was examined whether participants had spontaneously used a sequential egocentric strategy, an allocentric strategy, or a mixed strategy to locate the goal. The allocentric task specifically tested children’s capability to use an allocentric strategy. It should be noted that only half of the 5-year-olds learned the task due to concentration issues. Hence, for the analyses, only the children who managed to learn the training route themselves or managed to do so

Discussion

In this study, 5-, 7-, and 10-year-olds were tested in the virtual StarMaze task (Iglói et al., 2009). This experimental design assesses participants’ spontaneous or imposed use of sequential egocentric and allocentric strategies during navigation. Two tasks were performed: the multiple strategies task (composed of training and probe trials) and the “forced” allocentric task. In the training trials, participants needed to learn a fixed route to a goal. In the probe trials, the departure changed

Acknowledgments

This work was supported by an EU NEST Fp6 grant (12959, Wayfinding), the Fondation pour la Recherche Medicale (FRM), the UPMC, and the ANR young researcher program (DLC20060206428) to L.R.-R. We thank the children from the Woutertje Pieterse primary school in Leiden, Netherlands, who participated in this study.

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