Psychological Research DOI 10.1007/s00426-015-0658-9

ORIGINAL ARTICLE

Development of egocentric and allocentric spatial representations from childhood to elderly age Gennaro Ruggiero1 • Ortensia D’Errico1 • Tina Iachini1

Received: 8 August 2014 / Accepted: 28 February 2015 Ó Springer-Verlag Berlin Heidelberg 2015

Abstract 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

& Gennaro Ruggiero [email protected] 1

Laboratory of Cognitive Science and Immersive Virtual Reality, Department of Psychology, Second University of Naples, Viale Ellittico, 31, 81100 Caserta, Italy

structural and functional changes due to incomplete maturation (in youngest children) and deterioration (in oldest adults) of underlying cerebral areas.

Introduction Spatial memory plays a fundamental role in daily-life abilities such as way-finding and localizing places. Spatial information is stored in human memory according to two classes of spatial frames of reference: egocentric and allocentric (Arnold et al., 2013; Burgess, 2006; Iachini, Ruggiero, Conson, & Trojano, 2009b; O’Keefe & Nadel, 1978; Paillard, 1991; Piaget & Inhelder, 1967; Ruggiero, Frassinetti, Iavarone, & Iachini, 2014; for a review see Galati, Pelle, Berthoz, & Committeri, 2010). Egocentric frames of reference use the organism as the center of the organization of surrounding space. When an egocentric representation is formed, it is easier to retrieve spatial information from experienced than novel perspectives (e.g., Easton & Sholl, 1995; Iachini & Logie, 2003; Rieser, 1989; Roskos-Ewoldsen, McNamara, Shelton, & Carr, 1998; Vallar et al., 1999; Wang & Spelke, 2000). By contrast, allocentric frames of reference are centered on external objects or on the environment itself. For this reason, derived spatial representations are not dependent on the subjective vantage point and a difficulty to retrieve spatial information may emerge due to the need of detaching from the original egocentric perspective (e.g., Iachini, Ruotolo, & Ruggiero, 2009d; McNamara, 2003). Neurofunctional studies have overall reported activation of the posterior parietal/frontal network in egocentric processes and the posteromedial and medio-temporal cerebral substructures in allocentric processes (see Galati et al., 2010).

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Given the crucial role of spatial memory in our lifetime, the question arises of how spatial frames of reference develop from childhood to elderly age. As regards spatial memory during childhood, classic models have proposed a developmental course from initial egocentric/route to allocentric/survey representations (Acredolo, 1977, 1978; Piaget & Inhelder, 1967; Siegel & White, 1975; Thorndyke & Hayes-Roth, 1982). The developmental shift from egocentric to allocentric representations would be based on the children’s ability to combine perceptual experiences of an environment in such a way as to form a unitary spatial representation (Nardini, Thomas, Knowland, & Braddick, 2009; Vasilyeva & Lourenco, 2012). However, several studies have shown that even very young children have the capacity to rely upon allocentric cues, although the results obtained so far are not yet conclusive (Newcombe & Huttenlocher, 2003; Vasilyeva & Lourenco, 2012). For example, 3-/4-year-old children seem to have a basic ability to form allocentric representations if appropriately supported by environmental cues (Acredolo, 1977, 1978; Acredolo & Evans, 1980; Hermer & Spelke, 1994; Learmonth, Nadel, & Newcombe, 2002; Ribordy, Jabe`s, Banta Lavenex, & Lavenex, 2013). Nardini, Burgess, Breckenridge, and Atkinson (2006) assessed 3-/6year-old children on a task that manipulated egocentric/ allocentric representations between presentation and test. They found that both frames of reference were present in 5-year-old children (see also Newcombe & Huttenlocher, 2003). Bullens, Iglo´i, Berthoz, Postma, and Rondi-Reig (2010) tested spatial navigation abilities of 5-, 7-, and 10-year-old children by means of the StarMaze paradigm (Iglo´i, Zaoui, Berthoz, & Rondi-Reig, 2009). Results showed a gradual development from an egocentric to a more stable map-like representation between 5 and 10 years of age. While spatial strategies employed by adults are based on the parallel cooperation of egocentric and allocentric frames of reference (e.g., Nadel & Hardt, 2004), the capacity of children to efficiently integrate them seems to emerge at around 6 years of age (Bullens et al., 2010; Nardini et al., 2006; see also Nardini, Jones, Bedford, & Braddick, 2008). Some authors have suggested that this period is crucial for the development of executive functions that enable the acquisition of new skills such as selecting the appropriate spatial strategy and combining spatial and non-spatial environmental properties (Hermer & Spelke, 1994; Nardini et al., 2008, 2009; Vasilyeva & Lourenco, 2012). The improvement of executive functions is related to the slow maturation of the prefrontal cortex (e.g., Fuster, 2002; Giedd et al., 1999; Huttenlocher, 1979; Tsujimoto, 2008). However, it is not yet clear when these executive functions reach full maturity and when egocentric and allocentric frames of reference start cooperating efficiently in

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children (Nardini et al., 2008, 2009; Vasilyeva & Lourenco, 2012). As concerns the effect of aging on spatial memory, a decline in selective spatial abilities is often reported in healthy people; whereas severe spatial disorders are associated with neurodegenerative syndromes (for reviews see Iachini, Iavarone, Senese, Ruotolo, & Ruggiero, 2009a; Moffat, 2009). The age-related normal decline is often attributed to functional changes of the posteromedial, the medio-temporal and the frontal areas (Cabeza & Dennis, 2012; Lithfous, Dufour, & Despre´s, 2013; Moffat, 2009). Research carried out in the ‘real-world’ settings and involving healthy samples has shown a poorer allocentric performance of elderly people in comparison to young people in memorizing unfamiliar environments (Burns, 1999; Kirasic, 1991; Wilkniss, Jones, Korol, Gold, & Manning, 1997; see also Newman & Kaszniak, 2000). Studies based on the virtual maze paradigm have shown an age-related difficulty in spatial tasks requiring allocentric strategies (Iaria, Palermo, Committeri, & Barton, 2009; Jansen, Schmelter, & Heil, 2010; Picucci, Caffo`, & Bosco, 2009; Rodgers, Sindone III, & Moffat, 2012; for reviews see Klencklen, Despre´s, & Dufour, 2012; Lithfous et al., 2013; Moffat, 2009; but see Lemay, Bertram, & Stelmach, 2004). Iaria and co-workers (2009) compared young and old participants on a task requiring to generate and use a cognitive map acquired through virtual scenarios. Results showed that older participants were slower in forming a cognitive map and less accurate in using it than younger participants. Rodgers and colleagues (2012), by using a virtual maze task, found that older adults took a longer time than younger adults to solve the task. More recently, Montefinese, Sulpizio, Galati, and Committeri (2014) asked young and older adults to encode a target according to allocentric environment-based, allocentric object-based, and egocentric frames. Results revealed a difficulty of older people in both environment- and object-based allocentric encodings as compared to their younger counterparts. However, research has also shown a difficulty of elderly people in spatial tasks requiring egocentric encoding, such as route learning of complex real settings (Wilkniss et al., 1997), localizing goals and working out routes (Moffat, Zondermann, & Resnick, 2001), integrating paths (Harris & Wolbers, 2012; Mahmood, Adamo, Briceno, & Moffat, 2009) and recalling the temporal order of landmarks and directional information (Head & Isom, 2010). Therefore, it is not yet clear to what extent aging affects egocentric and allocentric frames of reference. In sum, previous literature suggests that the cooperation between egocentric and allocentric frames of reference seems more difficult during childhood and elderly age (for childhood: Vasilyeva & Lourenco, 2012; for aging: Lithfous et al., 2013). However, childhood and elderly age have

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been studied separately within the domain of spatial memory and, consequently, no data are available on the use of both frames of reference throughout the entire lifespan. Moreover, no study has assessed the development of these spatial frames by using the same spatial memory task. To the best of our knowledge, there was only one attempt to compare the performance of 8-year-old twins (mono-/dizygotic) on a virtual navigation task with data about young/ older adults collected from other studies (Bohbot et al., 2012). Results showed a preference for a landmark-based strategy in children and for an egocentric-based strategy in adults (for cross-sectional/longitudinal studies see Schaie, 2005). We deem, hence, that this lack in the literature might have limited a better understanding of the overall capability of processing spatial frames of reference in a lifespan perspective. The purpose of this research is to provide some preliminary data about the capacity of processing egocentric and allocentric frames of reference in a large sample of healthy participants including children, pre-adolescents, adolescents, and young, middle-aged, and older adults (aged from 6 to 89 years). Specific goals were: (1) tracing a baseline of the normal process of development, consolidation and decline of these spatial components; (2) clarifying if, and to what extent, egocentric and allocentric frames are differently vulnerable to the effect of age. All participants were submitted to a spatial memory task (‘‘Ego-Allo Task’’) based on the judgments of distances between objects placed in peripersonal (within arm reaching) and extrapersonal (outside arm reaching) spaces (Berti & Frassinetti, 2000; Iachini et al., 2009b). We also considered the peripersonal–extrapersonal dimension because frames of reference could have a different importance in these sectors of space. Peripersonal space defines the area where there is direct interaction between objects and body; in this area, stimuli are encoded according to egocentric frames of reference for the purpose of action guidance (e.g., Coello, Bourgeois, & Iachini, 2012; Iachini, Ruggiero, Ruotolo, & Vinciguerra, 2014a; Makin, Holmes, & Ehrsson, 2008; Rizzolatti, Fadiga, Fogassi, & Gallese, 1997). Hence, egocentric frames should be more important in peripersonal space than extrapersonal space, where objects are out of reach. The ‘‘Ego-Allo Task’’ was based on distance judgments that explicitly required either an egocentric or an allocentric reference frame. Response time and accuracy measured the performance. The task has already been used to assess spatial memory in healthy adults (Iachini & Ruggiero, 2006; Ruotolo, van Der Ham, Iachini, & Postma, 2011; Ruotolo, van der Ham, Postma, Ruggiero, & Iachini, 2015), brain-damaged patients (Iachini et al., 2009b; Ruggiero et al., 2014), blind people (Iachini, Ruggiero, & Ruotolo, 2014b; Ruggiero et al., 2009, 2012),

children with Cerebral Palsy (Barca, Frascarelli, & Pezzulo, 2012; Barca, Pezzulo, & Castelli, 2010) and has proved its efficacy in inducing a specific involvement of spatial frames of reference. On the basis of the literature, we hypothesized a difficulty, in terms of lower accuracy and longer processing time, with both spatial judgments in younger children and older adults (Montefinese et al., 2014; Vasilyeva & Lourenco, 2012). Furthermore, we expected an interaction between the space sector and the frames of reference: in peripersonal space a facilitation for the egocentric rather than allocentric encoding should emerge. Finally, age could also modulate these effects— that is, a difficulty in the allocentric component of extrapersonal space could emerge in younger children and older adults (e.g., Bullens et al., 2010; Lithfous et al., 2013; Montefinese et al., 2014).

Methods Participants A total of 283 healthy participants, 146 females, took part in the experiment. On the basis of their age, they were assigned to 12 groups (ranging from 6 to 89 years of age) as follows: 6–7, 8–9, 10–12, 13–15, 16–19, 20–29, 30–39, 40–49, 50–59, 60–69, 70–79, and 80–89. The number of males and females within each age group was balanced (the only differences were due to one more female in some groups) (see Table 1). No gender differences on overall age appeared [F (1, 281) = 1.122, p = 0.29]. Adults (starting from 20 years) were first submitted to a test of general cognitive abilities, the Mini Mental State Examination (MMSE; Folstein, Folstein, & McHugh, 1975; Iavarone et al., 2007; Measso et al., 1993). No one reported a score below 28 (MMSE 29.71, SD 0.34; cut off 23.8). All participants were free from neurological and psychiatric disorders as reported by detailed medical history. All participants had normal or corrected-to-normal vision. They were explicitly asked to report possible perceptual—that is, visual or hearing, deficits (for minors, their parents were interviewed). Elderly participants were recruited from doctor’s offices of several cities of Campania (Italy). Most of the younger participants were recruited from the local schools, universities and public places via advertisements and by word of mouth. The experimenters who ran the experiment and all participants were blind to the hypotheses of the study. All participants gave written consent to take part in the study. In the case of minors’ participation, written consent was obtained from the parents. Participants’ recruitment and testing was in conformity with the relevant local Ethics Committee requirements.

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Psychological Research Table 1 Means and standard deviations (SD) of accuracy and response time for egocentric and allocentric spatial judgments of each age group

Age groups (years)

Male

Accuracy (0–1)

Response time (s)

Egocentric Mean (SD)

Allocentric Mean (SD)

Egocentric Mean (SD)

Allocentric Mean (SD)

6–7

11

11

0.60 (0.27)

0.47 (0.23)

2.99 (1.27)

5.26 (2.75)

8–9

10

11

0.76 (0.22)

0.59 (0.25)

1.82 (1.01)

2.66 (1.33)

10–12

12

13

0.80 (0.20)

0.57 (0.25)

1.58 (0.81)

2.15 (1.00)

13–15

10

11

0.83 (0.15)

0.60 (0.30)

1.24 (0.52)

1.54 (0.86)

16–19

11

12

0.86 (0.12)

0.63 (0.28)

1.43 (0.46)

1.96 (1.03)

20–29

12

13

0.90 (0.13)

0.60 (0.32)

1.64 (0.53)

2.46 (1.08)

30–39 40–49

13 12

14 13

0.86 (0.21) 0.86 (0.18)

0.66 (0.27) 0.63 (0.26)

1.97 (1.02) 1.74 (0.71)

3.15 (1.47) 3.13 (1.18)

50–59

11

12

0.86 (0.14)

0.61 (0.29)

2.10 (1.03)

4.01 (1.59)

60–69

11

12

0.75 (0.18)

0.60 (0.25)

2.45 (1.39)

3.80 (1.75)

70–79

12

12

0.68 (0.25)

0.59 (0.30)

2.59 (1.48)

4.14 (2.12)

80–89

12

12

0.62 (0.23)

0.50 (0.25)

2.65 (1.30)

5.23 (2.60)

Materials and stimuli The experiment was carried out in a sound-proofed comfortable room of the Laboratory of Cognitive Science and Immersive Virtual Reality (Department of Psychology, SUN, Italy). Materials and procedure were the same as in Iachini and Ruggiero (2006), Iachini et al. (2009b), Iachini et al. (2014b) (Ruggiero et al., 2014). The stimuli comprised easily nameable and well-known 3D geometrical objects such as pyramid, parallelepiped, cone, cube, sphere, and cylinder presented in two sizes: big (8 9 8 cm, except parallelepiped and cylinder: 8 9 11 cm) and small (6 9 6 cm, except parallelepiped and cylinder: 6 9 9 cm). The objects differed in color: dark, medium and light gray. By combining objects, size and color, 18 objects were selected (e.g., the cone could be big, dark, etc.). The 18 objects were subdivided into two series (A: pyramid, parallelepiped, and cone; and B: cube, sphere, and cylinder). Still, each series was subdivided into 3 triads. Each triad had a target object (T), that is the object with respect to which the allocentric judgments were given. Each triad was arranged on the desk on a plasterboard panel (50 cm 9 30 cm 9 2 cm) according to the following criteria: (1) inter-object metric distances had to be easily distinguishable; (2) the metric distances were established in such a way that the amount of metric difficulty was the same for egocentric and allocentric judgments. The metric difficulty was related to the amount of distance between stimuli. Examples of triads and related inter-object and participant-object distances are given in Fig. 1a, b. In Fig. 1a, the distances between the stimuli were: parallelepiped–pyramid = 13 cm; pyramid–cone = 21 cm; cone–parallelepiped = 33 cm. The parallelepiped and cone were, respectively, 15 and 7 cm far from the body.

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Female

The pyramid was the target (i.e., the point of reference) for the allocentric judgments. The metric difference between the two objects closer to the body was 8 cm (15–7) and corresponded to that of the two objects closer to the pyramid (21–13). In Fig. 1b, the distances were: cube– sphere = 11 cm, sphere–cylinder = 17 cm, cylinder– cube = 28 cm; cube and cylinder were, respectively, 12 and 6 cm far from the body. The sphere was the allocentric-target object. The metric difference between the two objects closer to the body was 6 cm (12–6) and was the same as the difference between the sphere and the other two objects (17–11). In another triad, the distances were the following: sphere–cylinder = 22 cm; cylinder– cube = 12 cm; cube–sphere = 32 cm; allocentric target = cylinder; sphere and cube were 4 and 14 cm far from the body; egocentric and allocentric metric difficulty corresponded to 10 cm. The remaining triads were arranged similarly to the examples reported here and their metric difficulty ranged from 5 to 10 cm. The arrangement of the materials was based on the pilot studies presented in previous reports (Iachini & Ruggiero, 2006; Iachini et al., 2009b). Furthermore, a possible artifact could affect the task: the egocentric frame was known in advance, while the allocentric one was not. This criticism has been addressed in control experiments reported previously (Iachini & Ruggiero, 2006, Exp. 2; see also Ruotolo et al., 2015). Participants had to study six triads of objects from six different positions: in this way, egocentric and allocentric frames of reference varied for each configuration. Results confirmed the advantage of the egocentric component on the allocentric one. To guarantee that all triads were presented in the same way for all participants, each triad was presented in front of the participants by means of a panel with the same size as the desk (see again Fig. 1a, b). On this panel, the shape forming the basis of each object was

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Fig. 1 a, b Examples of materials and procedure of the Ego-Allo task. On the left, a illustrates an example of triad of the series A (i.e. pyramid, parallelepiped, and cone); on the right, b illustrates an example of triad of the series B (i.e. cube, sphere, and cylinder). The objects are placed on a plasterboard panel covering the desk. The panel is placed centrally in correspondence of participant’s midsagittal plane at 30 cm from the edge of the desk. ‘‘T’’ represents the

target-object (e.g., in a the pyramid; in b the sphere) that is the point of reference used to provide the allocentric judgments. Black dashed lines indicate relative distances between objects (e.g., in a cone– pyramid; in b cube–sphere) and between participants’ position and the objects (e.g., in a participant–parallelepiped; in b participant– cylinder)

engraved and the corresponding object was placed there. The triads were presented in two portions of space: peripersonal and extrapersonal. In the peripersonal space condition, the panels were placed within arm-reaching space—that is, ranging from 20 cm (from the edge of the desk) for younger children to 30 cm for all remaining groups. In the extrapersonal space condition, the panels were positioned out of the arm-reaching space—that is, ranging from 50 cm (from the edge of the desk) for younger children to 100 cm for all remaining groups.

Learning phase

Procedure At the beginning of the experiment, all participants received written instructions about the task that were then orally repeated by the experimenter. All participants understood the instructions without difficulty. They were instructed to memorize as accurately as possible the positions and the characteristics of the objects. Then, there was a training session in which an example of the entire procedure by means of three common objects (e.g., a white glass, a red cup and a black small box) was given. Besides the spatial judgments, the training session also included visual judgments (regarding color and size of objects) to exclude the presence of visual deficits. Once the procedure was clear, the experiment started.

At the beginning of each trial, three objects were randomly aligned in parallel with the edge of the desk and named to exclude possible effects due to difficulties in recognizing and naming the objects. Children were asked whether they knew the geometrical figures and, to avoid problems due to difficulty of naming, they were also asked to name the stimuli. During the entire experimental session, these same names were used by the experimenter (for example, ball instead of sphere). Then, while participants were asked to keep their eyes closed, the experimenter arranged the triad on the desk by means of the proper panel. Afterwards, participants had to open their eyes and to memorize the objects and their characteristics (20 s). Finally, participants had to close their eyes again and the experimenter removed the triad. After 5 s, the testing phase began. Testing phase Participants were asked to verbally provide eight judgments for each triad, for a total of 48 trials. For each triad, there were two egocentric questions—that is, ‘‘Which object was closest/farthest to you/from you?’’; two allocentric questions—that is, ‘‘Which object was closest/farthest to/ from the cone (allocentric target)?’’; and four distractor questions about characteristics of objects: two regarding

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the size—that is, ‘‘Which object was the tallest/lowest?’’; two regarding the color—that is, ‘‘Which object was the darkest/clearest?’’. The last questions were meant to discourage learning strategies based on the verbalization of the spatial relations. Verbalization of the spatial relations would be a potential problem as this could mask the differential influences of spatial memory factors, such as alloversus egocentric framing or far versus near space locations. Peri-/extrapersonal spaces and the order of presentation of the triads were balanced across participants. The order of presentation of the questions was first randomized and then balanced across subjects on the basis of a Latin square design. The experiment lasted approximately 20 min. The time (in sec) required to give each spatial judgment was recorded from when the experimenter announced the implied frame of reference (body or target object) until participants gave the response—that is, the time between the end of the question and the beginning of the answer. The experimenter used a handheld stopwatch to record the scanning time. For each judgment accuracy (1 = correct; 0 = incorrect) was recorded. For each condition (i.e., reference frames combined with space sectors), mean accuracy and mean response time were computed. At the ending of the testing phase, participants were interviewed to be sure that they had followed the instructions accurately. Statistical analyses Two 12 9 2 9 2 mixed ANOVAs that treated age groups as a 12-level between-subject factor (age groups: 6–7, 8–9, 10–12, 13–15, 16–19, 20–29, 30–39, 40–49, 50–59, 60–69, 70–79, and 80–89), egocentric-allocentric frames of reference as a 2-level within-subject factor (reference frame) and peripersonal–extrapersonal spaces as a 2-level withinsubject factor (space sector) were performed on accuracy and response time. The Unequal N HSD test was used to analyze post hoc effects and the magnitude of the significant effects was indicated by partial eta squared (g2p ). The effect of age on judgments about non-spatial object characteristics—that is, size and color—was also analyzed by means of two separate ANOVAs with groups as factor. Moreover, separate ANOVAs were carried out to check the effect of gender on spatial processing. Finally, to exclude speed–accuracy trade-off effects, a Pearson correlation between accuracy and response time for each condition (Ego-Peri, Allo-Peri, Ego-Extra, Allo-Extra) was performed. Means and standard deviations of each age group for egocentric and allocentric spatial components are shown in Table 1.

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Results Analyses on response time The ANOVA showed a significant main effect of age groups [F (11, 247) = 15.772, p \ 0.001, g2p = 0.41]. The post hoc tests confirmed that the effect was due to 6- to 7-year-old children and 80- to 89-year-old participants taking a longer time (p \ 0.001) than all other groups, except adults between 50 and 79 years. Besides this clear effect, post hoc tests showed that participants aged from 10 to 29 years performed faster than adults from 50 to 89 years (p \ 0.05). The space sector factor was significant: F (1, 11) = 14.155, p \ 0.001, g2p = 0.05, with judgments about peripersonal space (M 2.54, SD 1.58) being faster than those about extrapersonal space (M 2.84, SD 1.80). The ANOVA also showed a significant reference frame main effect: F (11, 247) = 242.662, p \ 0.001, g2p = 0.50. Egocentric judgments (M 2.04, SD 1.15) were faster than allocentric judgments (M 3.35, SD 2.22). These main effects were qualified by a significant age groups 9 reference frame interaction: F (11, 247) = 6.422, p \ 0.001, g2p = 0.22. As illustrated in Fig. 2, the effect shows a symmetrical U-shaped line with the youngest and the oldest participants representing the peaks of the U. The post hoc analysis showed that in giving allocentric judgments 6- to 7-year-old children and 80- to 89-year-old adults were slower than all remaining groups in both egocentric and allocentric judgments (at least p \ 0.001), except allocentric judgments provided by adults aged from 50 to 79 years. Finally, egocentric judgments of 13- to 15-year-old participants were faster than egocentric judgments of 6- to 7-year-old children (p \ 0.05) and 70- to 89-year-old adults (at least p \ 0.05). A further interaction between space sector and reference frame emerged [F (1, 247) = 4.399, p \ 0.05, g2p = 0.02]. The post hoc tests revealed that allocentric judgments in extrapersonal space were slower than all other conditions (at least p \ 0.001); allocentric judgments in peripersonal space were slower than egocentric judgments in both spaces (p \ 0.001); instead, no significant difference between egocentric judgments in both spaces emerged. The related means were: Peri-Ego 1.96, SD 1.16; Peri-Allo 3.13, SD 2.0; Extra-Ego 2.11, SD 1.15; Extra-Allo 3.56, SD 2.45. Furthermore, a significant 3-way age groups 9 reference frame 9 space sector interaction emerged: F (11, 247) = 1.973, p \ 0.05, g2p = 0.08 (see Fig. 3). The post hoc tests showed that the allocentric component in extrapersonal space took a longer time in 6- to 7-year-old children than all other judgments in remaining groups (at

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Fig. 2 Mean of response time (s) for egocentric and allocentric spatial judgments as a function of 12 age groups

Egocentric judgments Allocentric judgments

Response time (sec)

6

5

4

3

2

1

0 6/7

8/9

10/12 13/15 16/19 20/29 30/39 40/49 50/59 60/69 70/79 80/89

Age groups (years)

9 Egocentric judgments Allocentric judgments

8

Response time (sec)

7 6 5 4 3 2 1 0

6/7

10/12 16/19 30/39 50/59 70/79 8/9 13/15 20/29 40/49 60/69 80/89

Peripersonal space

6/7

10/12 16/19 30/39 50/59 70/79 8/9 13/15 20/29 40/49 60/69 80/89

Extrapersonal space

Fig. 3 Mean of response time (s) for egocentric and allocentric spatial judgments related to peripersonal and extrapersonal space as a function of 12 age groups

least p \ 0.01), except 80- to 89-year-old people. Similarly, 80- to 89-year-old people were slower than all other conditions apart from all allocentric judgments in adults aged from 50 to 79 years. Moreover, neither a main effect of gender [F (1, 257) = 1.700, p = 0.20] nor significant interactions

between gender 9 reference frame (F \ 1), gender 9 space sector (F \ 1), and gender 9 reference frame 9 space sector (F \ 1) appeared. Finally, no age effect was found on visual features of stimuli: size [F (11, 247) = 0.911, p = 0.53] and color [F (11, 247) = 0.875, p = 0.57].

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Analyses on accuracy The ANOVA showed a significant main effect of age groups [F (11, 262) = 8.549, p \ 0.001, g2p = 0.26]. The post hoc analysis showed that 6- to 7-year-old children were less accurate than all other groups (at least p \ 0.05) except adults in their seventies and eighties. Similarly, 80to 89-year-old adults were less accurate than all other groups (at least p \ 0.05) except 6- to 7- and 8- to 9-yearold children and 70- to 79-year-old adults. Egocentric judgments were significantly more accurate than allocentric ones [F (1, 262) = 215.884, p \ 0.001, g2p = 0.45], as shown by related means: egocentric 0.78, SD 0.22; allocentric 0.59, SD 0.27. These main effects were qualified by a significant age groups 9 reference frame interaction [F (11, 262) = 1.844, p \ 0.05, g2p = 0.07]. As it is illustrated in Fig. 4, the results form a reversed U-shaped line and thus strikingly mirror the pattern that emerged in RT, with a more robust impact of age on the egocentric component. Indeed, there were no significant differences among groups in allocentric judgments, apart from a tendency for young adults in their thirties performing better than 6- to 7-year-old children (p = 0.06) and 80- to 89-year-old adults (p = 0.09). In egocentric judgments, 6- to 7-year-old children and 80- to 89-year-old adults performed worse than participants from 10 to 59 years (at least p \ 0.05). Finally, 70- to 79-year-old adults were less accurate than young adults from 20 to

40 years (at least p \ 0.05) and a similar tendency was found for the difference to adults in their fifties (p = 0.07). Furthermore, neither a main effect of space sector (F \ 1), nor significant interactions between age groups and space sector (F \ 1) and age groups 9 reference frame 9 space sector (F \ 1) emerged. As regards gender, only a significant main effect of gender [F (1, 272) = 4.028, p \ 0.05] emerged, due to male participants (M 0.70, SD 0.24) being overall more accurate than female participants (M 0.67, SD 0.25). No other significant interactions (gender 9 reference frame: F \ 1; gender 9 space sector: F \ 1; gender 9 reference frame 9 space sector: F \ 1) appeared. Finally, no age effects were found on visual features of stimuli: size [F (11, 247) = 0.866, p = 0.57] and color [F (11, 247) = 1.654, p = 0.09]. Correlation analyses As regards the correlation analysis, the accuracy of the Ego-Peri condition correlated negatively with RTs of all other conditions: Ego-Peri (r = -0.31), Allo-Peri (r = -0.23), Ego-Extra (r = -0.30), Allo-Extra (r = -0.26). The accuracy of the Allo-Peri condition correlated negatively with RTs of the Ego-Peri (r = -0.19) condition. The accuracy of the Ego-Extra condition correlated negatively with RTs of all other conditions: Ego-Peri (r = -0.24), Allo-Peri (r = -0.20), Ego-Extra (r =

1,1

Fig. 4 Mean of accuracy (0–1) for egocentric and allocentric spatial judgments as function of 12 age groups

Egocentric judgments Allocentric judgments

1,0

Accuracy (0-1)

0,9

0,8

0,7

0,6

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10/12 13/15 16/19 20/29 30/39 40/49 50/59 60/69 70/79 80/89

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-0.23), Allo-Extra (r = -0.22). The RTs of the AlloExtra combination showed no significant correlation with accuracy. Therefore, the better the egocentric performance about peripersonal and extrapersonal spaces the faster the overall RTs. In any case, no speed–accuracy trade-off effects were found.

Discussion Spatial frames of reference are fundamental in our daily life to remember the position of objects or places and find the way. Given their theoretical and clinical relevance, much research has tried to clarify the capacity to process these spatial frames in childhood and elderly age but an overview that comprises the entire life span is still missing. In this study, the developmental course of spatial frames of reference from childhood to elderly age—that is, healthy people from 6 to 89 years—was investigated through the same spatial memory task. The task required egocentric and allocentric verbal spatial judgments related to objects placed in peripersonal and extrapersonal spaces (Iachini & Ruggiero, 2006; Iachini et al., 2009b). Results showed that egocentric judgments were more accurate and faster than allocentric judgments. Moreover, frames of reference interacted with the sector of space: allocentric judgments in extrapersonal space were slower than all other conditions, while egocentric judgments were faster than allocentric ones in both spaces. The correlation analysis also revealed that the egocentric accuracy in both spaces correlated negatively with the speed of processing of all other conditions, and this seems to suggest that the egocentric level of ability plays a special role in the spatial encoding. The overall facilitation of the egocentric component may reflect the primacy of the egocentric frame in human beings (Delius & Hollard, 1995; Millar, 1994). Humans, because of their ground-bound upright stance, have an egocentric or perspective-mediated interface with the environment (Delius & Hollard, 1995; McNamara, 2003; Millar, 1994). With regards to gender differences, we found that male participants were overall more accurate than female participants. This male advantage is consistent with much research reported in previous literature (e.g., Coluccia & Louse, 2004; Iachini et al., 2009d). As regards the impact of age on general spatial representations, younger children (6–7 years) and older participants (80–89 years) were slower and less accurate than other age groups. Indeed, the results showed a slowing of processing time starting at 50 years and becoming progressively more evident as age increased until 89 years. The slowing was also found in younger children. Moreover, 6- to 7-year-old children were less accurate than all

other groups except adults from 70 to 89 years of age. Similarly, 80- to 89-year-old adults were less accurate than all other groups except adults in their seventies. Therefore, the level of accuracy looked quite homogeneous between 10 and 60 years of age, with a decline starting at about 70 years. This may suggest that during this long period, an efficient spatial processing is ensured by having the two frames of reference cooperating in parallel (Nadel & Hardt, 2004). In sum, when considering general spatial judgments, the patterns of accuracy (forming a reversed U shape) and response time (forming a U shape) showed a mirror-like developmental line with the youngest children and oldest adults performing in a strikingly similar way. One could except that these effects may simply reflect a general age-related decline. However, the analysis of judgments on color and size of the objects revealed no significant influence of age. This reinforces the idea that aging exerts a selective influence on spatial frames of reference, but not on the general ability to retrieve purely visual and visuo-spatial (size) features (see also Iachini, Poderico, Ruggiero, & Iavarone, 2005). Results, then, confirm a difficulty with both spatial judgments, but not with judgments about non-spatial object characteristics, in younger children and older adults. However, when considering the effect of age on egocentric and allocentric spatial judgments, the patterns of accuracy and response time look less homogeneous. As regards response time, each spatial component replicated the U-shaped line of the general effect of age but the slowing was more evident in the allocentric component (see Fig. 2). Indeed, 6- to 7-year-old children and 80- to 89-year-old adults were slower than other groups. As expected, the effect was particularly strong in extrapersonal space (see Fig. 3). The overview of the data shows that the allocentric slowing started at about 50 years and progressed as age increased (see also Raz, Rodrigue, Head, Kennedy, & Acker, 2004). This is consistent with previous research reporting a slowing of the allocentric processing time in elderly people (Iachini, Ruggiero, & Ruotolo, 2009c; Klencklen et al., 2012; Lemay et al., 2004; Lithfous et al., 2013; Moffat, 2009; Montefinese et al., 2014; Rodgers et al., 2012) and in early childhood (Bullens et al., 2010; Vasilyeva & Lourenco, 2012). As regards accuracy, each spatial component replicated the reversed U-shaped line of the general effect of age but this time, the impact was more evident on the egocentric component (see Fig. 3). Indeed, younger children (6–7 years) and older adults performed similarly and less accurately than participants from 10 to 59 years of age. The level of egocentric ability started decreasing at about 60 years and continued progressively with a clear drop during the eighties. This is in line with the literature

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showing egocentric difficulties with increasing age in healthy people (Head & Isom, 2010; Iachini et al., 2009a, c; Moffat et al., 2001; Wilkniss et al., 1997). It is also consistent with research suggesting that the period comprised between 7 and 9 years is crucial for the consolidation of spatial memory abilities (Bullens et al., 2010; Newcombe & Huttenlocher, 2003; Vasilyeva & Lourenco, 2012). In sum, the egocentric performance was very accurate (with accuracy [85 %) and similar from 16 to 59 years, with a peak during the twenties. Instead, there were no robust differences among groups in allocentric accuracy with percentages ranging from 47 to 66 %, in line with previous literature (Pouliot & Gagnon, 2005). The correlation analysis showed no evidence of speed– accuracy trade-off: this may reflect the fact that during the developmental course, the level of allocentric accuracy stayed quite low and constant, while the latency of egocentric memory judgments stayed quite short and constant. Considering accuracy and response time, these measures represent complementary aspects of the same performance (Lohman, 1989, 2000). Clearly, response time reflects the speed and the types of processes involved, while the level of ability is reflected by accuracy and can also be linked to RT. For example, a high level of ability may produce high accuracy and short RT. However, a person may be able to perform sufficiently well by a longer RT. This seems to be the case of the allocentric performance in younger children and older adults and might explain why there is no significant effect of age on the allocentric accuracy. One way to cope with the age-related allocentric difficulty is to remodulate the spatial processing by relying more on the egocentric components (see Lithfous et al., 2013). As a consequence, the allocentric processing should take a longer time, while the egocentric processing could lose accuracy. We must recognize, however, that depending on the spatial task either an egocentric or an allocentric difficulty (or both) could emerge. The present allocentric task requires an object-based intrinsic frame. In the literature, tasks such as simulated navigation (e.g., Bullens et al., 2010; Moffat et al., 2001, 2009), view changing tasks in virtual environments (Montefinese et al., 2014), topographical learning of complex large-scale indoor (e.g., Barrash et al., 1998; Maguire et al., 1998; Wilkniss et al., 1997) or outdoor (e.g., Epstein, 2008) environments were often adopted. It is possible that the scale of space (i.e., large-scale locomotor vs small-scale manipulatory) and the characteristics of the task (requiring navigational abilities, path exploration, map learning or object location) make a difference (on this point see Iachini & Ruggiero, 2010; Iachini, Ruggiero, & Ruotolo, 2014a). The allocentric processing could be more demanding and more sensitive to age-related variations when it is concerned with large-scale

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environmental frames and navigational abilities. However, the present task was recently adopted to study topographical disorientation in a brain-lesioned patient (Ruggiero et al., 2014). Results showed that this small-scale space task was able to detect alterations of specific components of spatial memory responsible for topographical disorientation. Coming back to the pattern of results, how can we explain the symmetry between the youngest children and the oldest adults regarding the level of accuracy and the amount of processing time? We argue that this symmetry reflects the process of maturation (in childhood) and the deterioration (in aging) of the same cerebral areas underlying spatial memory. Spatial memory efficiency is associated with structural and functional integrity of the spatial memory neural network (i.e., hippocampus, parahippocampal gyrus, retrosplenial, postero-cingulate cortex, parietal lobe and frontal areas) that involves the allocentric encoding (hippocampus and surrounding areas) and also executive functions (Burgess, 2008; Cabeza & Dennis, 2012; Galati et al., 2010; Iachini et al., 2009a; Moffat, 2009; Vann, Aggleton, & Maguire, 2009). Much research has documented that normal aging is characterized by reductions in the volume of the hippocampus and the frontal cortex, such as to produce allocentric (e.g., Rodgers et al., 2012) and egocentric (e.g., Head & Isom, 2010; Wilkniss et al., 1997) difficulties and a general decline in executive and attentional functions (Iachini et al., 2009a; Lithfous et al., 2013; Salthouse, 1996). Executive functions are necessary to acquire, combine and select spatial strategies, to plan and monitor behavioral motor responses according to environmental requirements (Lithfous et al., 2013; Vasilyeva & Lourenco, 2012). Some evidence has indeed reported strong associations between egocentric encoding and executive functions (e.g., Borella, Carretti, & De Beni, 2008; Iachini et al., 2005; Lithfous et al., 2013; Ruggiero, Sergi, & Iachini, 2008; Sanders, Holtzer, Lipton, Hall, & Verghese, 2008; see also Cornoldi & Vecchi, 2003; Craik, 1986; Meneghetti, Fiore, Borella, & De Beni, 2011; Park, 2000). Similarly, in childhood, the capacity to efficiently use reference frames would occur at about 6 years or later (Nardini et al., 2008, 2009; Vasilyeva & Lourenco, 2012), as a consequence of delayed maturation of hippocampus and surrounding areas and frontal lobes as proved by myelination process, gray matter reduction, synaptogenesis, and resting metabolism (e.g., Fuster, 2002; Lenroot & Giedd, 2006; Newcombe & Huttenlocher, 2003; Pfefferbaum et al., 1994; Tsujimoto, 2008). Summarizing, the process of development (in children) and deterioration (in older adults) of hippocampal areas provokes in both groups a slowing in using cognitive maps. This slowing might lead to a shift from an allocentric to an

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egocentric strategy which causes an excessive cognitive demand for the frontal areas that are maturating in children and deteriorating in elderly people. The different impact of aging on spatial frames of reference confirms that egocentric and allocentric frames form specialized and interactive functions underpinned, at least partially, by neural areas that are differently vulnerable to normal aging processes (Arnold et al., 2013; Galati et al., 2010; Iachini et al., 2009a, b, c; Montefinese et al., 2014; Ruggiero et al., 2014). Finally, providing a baseline of the developmental course of egocentric and allocentric frames encoding may be useful for clinical purposes. Several studies have shown alterations of egocentric and allocentric spatial components in several neurodegenerative diseases. For example, Hort et al. (2007) compared healthy elderly people, patients suffering from Alzheimer’s disease (AD) and several subtypes of mild cognitive impairment (MCI) on a task requiring egocentric and allocentric encodings. Results revealed a deficit of the allocentric component in AD and amnesic-MCI patients (see also Dawson, Anderson, Uc, Dastrup, & Rizzo, 2009; Laczo´ et al., 2012). This suggests that a severe drop in the allocentric capacity could be a prodromic sign of a neurodegenerative disease (Hort et al., 2007; Iachini et al., 2009a). In conclusion, this study collected some preliminary data on the capacity to process spatial frames of reference in a large sample of healthy participants from childhood to elderly age (6–89 years). In this way, a comprehensive overview of the developmental course of this basic spatial capacity was provided. Egocentric and allocentric spatial representations were affected by age. A slowing in the processing time of the allocentric component in children of 6–7 years and in older adults (from 50 years and onward with a peak at 80–89 years) appeared. Besides, the level of egocentric accuracy was lower in children of 6–7 years and started to progressively decrease at about 60 years with a clear drop at 80–89 years. This clear symmetry in the behavioural outcomes of younger children and older people suggests that the incomplete maturation (in children) and the deterioration (in older adults) of the neural areas underlying spatial encodings may limit the capacity to combine, translate and use egocentric and allocentric spatial information. Further studies should explore the role of specific spatial processes and additional executive factors in determining age-related effects.

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