Research in Developmental Disabilities 38 (2015) 97–107

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Explorative function in Prader–Willi syndrome analyzed

through an ecological spatial task

F. Foti a,b, D. Menghini c, L. Petrosini a,b, S. Vicari c, G. Valerio d, E. Orlandi c,A. Crino e, S. Spera e, P. De Bartolo b,f, L. Mandolesi b,d,*a Department of Psychology, University ‘‘Sapienza’’, Via dei Marsi 78, 00185 Rome, Italyb IRCCS Santa Lucia Foundation (CERC), Via del Fosso di Fiorano 65, 00143 Rome, Italyc Child Neuropsychiatry Unit, ‘‘Children’s Hospital Bambino Gesu’’, Piazza Sant’Onofrio 4, 00165 Rome, Italyd Department of Motor Science and Wellness, University ‘‘Parthenope’’, Via Medina 40, 80133 Naples, Italye Pediatric and Autoimmune Endocrine Disease Unit, ‘‘Children’s Hospital Bambino Gesu’’, Via Torre di Palidoro, 00050 Fiumicino (Rome),

Italyf Faculty of Formation Science, University ‘‘Guglielmo Marconi’’, Via Plinio 44, 00193 Rome, Italy

A R T I C L E I N F O

Article history:

Received 9 September 2014

Accepted 28 November 2014

Available online

Keywords:

Spatial task

Explorative strategies

Genetic syndromes

Spatial memory

Spatial ability

A B S T R A C T

This study was aimed at evaluating the spatial abilities in individuals with Prader–Willi

syndrome (PWS) by using an ecological large-scale task with multiple rewards. To

evaluate the extent of spatial deficit in PWS individuals, we compare their performances

with those of individuals with Williams Syndrome (WS) in which the spatial deficits have

been widely described. Participants had to explore an open space to search nine rewards

placed in buckets arranged according to three spatial configurations: a Cross, a 3� 3

Matrix and a Cluster composed by three groups of three buckets each.

PWS individuals exhibited an explorative deficit in Cluster and Cross configurations,

while WS participants in Matrix and Cross configurations. The findings indicate that the

structural affordances of the environment influence the explorative strategies and can be

related to how spatial information is processed.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Prader–Willi syndrome (PWS) is a genetic disorder with an incidence rate at birth at about 1:15,000–1:20,000 caused byeither a paternal deletion within 15q11–q13 (70–75% of cases), or a maternal uniparental disomy of chromosome 15 (mUPD)(20–25%), or unbalanced translocation or imprinting center defect (2%) (Bittel, Kibiryeva, & Butler, 2006; Whittington et al.,2001). PWS is characterized by hyperphagia, early-onset and morbid obesity, hypogonadism, hypotonia, repetitive behavior,mental rigidity, impulsiveness, resistance to change, impaired social functioning (Ho & Dimitropoulos, 2010; Veltman, Craig,& Bolton, 2005) and by mild to moderate intellectual disability (ID) (Whittington et al., 2004). Their cognitive profile ischaracterized by strengths in long-term memory, visual perception, simultaneous processing, reading skill, and visuo-spatialfunctions, and weaknesses in attention, short-term memory, sequential processing, executive functions, action-based visualprocessing, auditory processing, mathematical skills, social cognition and language ability (Alvarez & Emory, 2006; Bertella

* Corresponding author at: Department of Motor Science and Wellness, University of Naples ‘‘Parthenope’’, Via Medina 40, 80133 Naples, Italy.

Tel.: +39 0815474771; fax: +39 0815474771.

E-mail address: laura.mandolesi@uniparthenope.it (L. Mandolesi).

http://dx.doi.org/10.1016/j.ridd.2014.11.022

0891-4222/� 2014 Elsevier Ltd. All rights reserved.

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–10798

et al., 2005; Copet et al., 2010; Dimitropoulos, Ferranti, & Lemler, 2013; Foti, Menghini, et al., 2011; Foti, Petrosini, et al.,2011; Koenig, Klin, & Schultz, 2004; Lo, Siemensma, Collin, & Hokken-Koelega, 2013; Relkovic et al., 2010; State & Dykens,2000; Walley & Donaldson, 2005; Woodcock, Humphreys, Oliver, & Hansen, 2010). However, PWS does not present ahomogeneous cognitive profile, especially with regard to spatial domain. In fact, some studies evidenced that PWSindividuals show good performances on tasks linked to visuo-spatial processing (Dykens, 2002; Verdine, Troseth, Hodapp, &Dykens, 2008), while other researches described their impairment in localizatory memory (Woodcock, Humphreys, & Oliver,2009; Woodcock et al., 2010). Moreover, in an animal model of PWS good capacities of spatial learning have been reported(Muscatelli et al., 2000).

Recently, we have investigated the spatial abilities in PWS individuals by radial arm maze task (RAM) (Foti, Menghini,et al., 2011), an ecological instrument that permits to evaluate the mnesic and procedural components of spatial function(Mandolesi, Petrosini, Menghini, Addona, & Vicari, 2009a; Mandolesi, Addona, et al., 2009). Data obtained evidenced thepresence of deficits especially in spatial procedural components (Foti, Menghini, et al., 2011). However, in RAM theindividuals have to find the hidden rewards according to a fixed spatial configuration and then the searching strategies areforced by the preset number of alternative routes that constrain and limit the searching behavior. To overcome thislimitation in the present research it is seemed interesting to investigate the spatial abilities of PWS individuals in a large-scale task without any space constraint. In this spatial test the subject is free to move putting into action exploratorybehaviors that should adapt to the environment features. Thus, the environmental affordances influence the construction ofthe search strategies as well as the knowledge on where the rewards are (Foti, Spirito, Mandolesi, Aversano, & Petrosini,2007; Foti et al., 2010; Foti, Petrosini, et al., 2011). Namely, in the present study the participants had to explore an open spaceto search nine rewards hidden in buckets arranged according to three spatial configurations: a Cross, a 3� 3 Matrix, a Clustercomposed by three groups of three buckets each.

To determine whether the performance exhibited by PWS participants was specific to this population or whether it was anon-specific effect of the Intellectual Disability (ID), we compared PWS performances with those of a mental age- andgender-matched group of individuals with Williams syndrome (WS) exhibiting a specific impairment of the visuo-spatialabilities (Foti, Petrosini, et al., 2011; Mandolesi, Addona, et al., 2009; Vicari, Bellucci, & Carlesimo, 2006). The performances ofPWS and WS individuals were compared with those of a third mental age- and gender-matched group of typically developing(TD) children used as a nonsyndromic control.

2. Methods

2.1. Participants

Fifteen individuals with PWS, 13 individuals with WS (syndromic control group) and 13 TD participants (control group)matching the PWS and WS individuals for mental age (MA) and gender have been examined in the present study.Chronological (CA) and mental (MA) ages as well as IQ of all participants are reported in Table 1.

All pathological participants were part of a larger pool of individuals attending the Children’s Hospital Bambino Gesu forclinical and rehabilitative follow up and lived with their own families. In PWS and WS participants, the clinical diagnosis wasconfirmed by genetic investigation (FISH), which showed the paternal deletion on chromosome band 15q11–q13 in PWSsample and the deletion on chromosome band 7q11.23 in WS sample. All PWS participants had been receivingpharmacological treatment GH therapy for at least 3 years and were in euthyroidism. While TD children were individuallytested in a quiet garden of their schools, all syndromic participants were tested in a quiet garden of the Children’s HospitalBambino Gesu. The parents of participants gave informed written consent. The study was approved by local ethicalcommittee and was conducted according to the Declaration of Helsinki.

2.2. Behavioral assessment

A neuropsychological battery was administered to each PWS, WS and TD participants in two separate sessions over 2consecutive days; the test presentation order was randomized. In all groups, MA was evaluated with the L–M form of the

Table 1

Statistical comparisons of chronological age (CA), mental age (MA) and IQ among PWS, WS and TD groups (one-way ANOVA and Duncan’s post hoc

comparisons).

Group CA

Mean

(�SEM)

F(fd)

P

Post hoc

MA

Mean

(�SEM)

F(fd)

P

Post hoc

IQ

Mean

(�SEM)

F(fd)

P

Post hoc

PWS 17.03

(�2.04)

F(2,38) = 12.36

= .000073PWS vs. WS n.s.

PWS vs. TD = .00099WS vs. TD = .00009

6.03

(�.03)

F(2,38) = .71

n.s.

52.8

(�2.3)

F(2,38) = 121.63

= .00000001PWS vs. WS n.s

PWS vs. TD = .00006WS vs. TD = .00012

WS 21.06

(�2.06)

6.04

(�.03)

55.6

(�1.9)

TD 6.04

(�0.02)

6.04

(�.03)

101.9

(�3.1)

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107 99

Italian version of the Stanford-Binet Intelligence Scale (Bozzo & Mansueto Zecca, 1993). Furthermore, visuo-motor abilities(Developmental Test of Visual-motor Integration-VMI; Beery, 2000) and visuo-spatial short-term memory abilities (visuo-spatial span-VSS and visual-object span-VOS; Vicari, 2007) were explored in all groups.

2.3. Apparatus

The apparatus was located outdoors in a large garden and consisted of nine orange plastic buckets (18 cm wide� 28 cmhigh) containing the reward (a little colored ball). The buckets that had a swinging cover were arranged according to threedifferent spatial configurations described in Section 2.4. The apparatus was surrounded by extra-maze cues (trees, swings,benches, etc.) held in constant spatial relations throughout the experiment. The buckets were virtually numbered. Onlyduring the testing the subjects could see experimental setting or have physical access to it. To increase the motivation to pickup the rewards, at the end of each trial the subject received a reward (a coin) in exchange for all the colored balls found in thebuckets. None of the participants had had previous experience with apparatus.

2.4. Procedures

Spatial configurations were derived from preceding experimental studies demonstrating their reliability in emphasizingtask features (De Lillo, Visalberghi, & Aversano, 1997; De Lillo, Aversano, Tuci, & Visalberghi, 1998; Foti et al., 2007; Foti,Petrosini, et al., 2011; Valsecchi, Bartolomucci, Aversano, & Visalberghi, 2000). In the Cluster configuration, the buckets werearranged in triplets 1208 away from each other and buckets were placed 4 m apart. The minimal distance traveled to exploreall buckets was 42 m. In the Matrix configuration, the buckets were arranged in a 3� 3 square matrix, with buckets 4 m apartand the minimal distance traveled was 32 m. In the Cross configuration, the buckets were arranged in an ‘‘X’’ formation, withbuckets 4 m apart. In this case, the minimal distance traveled was 40 m.

Each participant was allowed to freely explore the apparatus to retrieve the rewards. A trial ended when all nine rewardshad been collected or 30 visits (correct or wrong) had been made. Since the buckets were never rewarded twice in the sametrial, the optimal performance consisted of visiting each bucket only once, collecting nine rewards through nine visits. Anerror was made when the subject re-visited a bucket already visited during the same trial. Each participant performed twotrials a day (inter-trial interval: 2 h) with a given spatial configuration. The successive day the subjects performed two trialswith another spatial configuration. Finally, the third day the participants performed two trials with the last spatialconfiguration. The order of presentation of the three configurations was counterbalanced among participants.

At the beginning of the first test day, the experimenter used the same simple verbal instructions to explain the task toeach participant (‘‘The game is to find some little colored balls. Do you see the orange buckets? You have to reach a bucket,take the little ball inside, until you have collected all the balls. Go and have fun!’’). No other instruction or verbalencouragement was provided during the testing. The participants’ behaviors during the trials were videotaped and recordedmanually. Each participant wore an actigraph device (wActiSleep-BT, ActiGraph, Pensacola, Florida) to record the stepsperformed during the exploration of each configuration.

2.5. Behavioral parameters

In each of the two trials of a given configuration, the following parameters were analyzed: search time, the time (inseconds) employed to complete the task; total errors, the percentage of total errors out of the total visits (considering eitherno-visits and re-visits, i.e. ignoring a bucket without visiting it so that it remained rewarded, or re-visiting a previouslydepleted bucket); error-free trials, the sum of trials in which subjects did not make any error; frequency of visits, the number ofvisits made to each bucket; spatial span, the longest sequence of correct visits; perseverations, the sum of times in which thesubject consecutively re-visited the same bucket in each trial (the re-visited bucket could be either the same bucket: i.e. 5-5,or the same sequence of maximum three buckets: i.e. 1-2-3-1-2-3). Perseverations on more than three buckets were neverobserved. Finally, we measured the length of the step of each participant to calculate the total distance traveled (in m).

In the Cluster configuration, further parameters were analyzed: number of clusters visited or revisited in each trial (beingthree the clusters of the configuration, this parameter ranged from the worst value of 30 to the best value of 3); number ofclusters depleted with three consecutive correct visits (this parameter ranged from the worst value of 0 to the best value of 3).Furthermore, the errors were classified as within-cluster errors, that is the revisits to a bucket belonging to the same clusterthe subject was visiting or across-cluster errors, that is, the late revisits to a bucket belonging to an already visited cluster inthe same trial.

2.6. Drawings

To evaluate the graphic and mental representative mapping abilities, after the second trial of each configuration, allsubjects were asked to make a drawing of the setting where they had just ‘‘played’’. Thus, each subject drew three drawings,one for each configuration. We obtained 45 drawings made by the 15 PWS individuals, 39 drawings made by the 13 WSindividuals and 39 drawings made by the 13 TD children. No instructions about representing the single objects or the globalsetting or about indicating how many buckets (or rewards) were present in the play was provided. In each drawing of the

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107100

three spatial configurations, shape of spatial configurations, cardinality (number of elements of the setting) and details ofobjects were evaluated.

2.7. Statistical analysis

Metric unit results of subjects belonging to all experimental groups were presented as mean values of the two trials of anyconfiguration� SEM, since in all parameters PWS, WS and TD groups did not display any significant difference between the firstand the second trial. The data were first tested for normality (Shapiro–Wilk’s normality test) and homoscedasticity (Levene’s test)and then compared using one- or two-way analyses of variance (ANOVAs) followed by post hoc multiple comparisons by usingDuncan’s test. The two-way ANOVAs were performed by applying the mixed model for independent variable (group) and repeatedmeasures (configurations). When parametric assumptions were not fully met, non-parametric ANOVAs (Kruskal–Wallis’ test (H-statistic) and Mann–Whitney’s U test; Z-statistic) were used. Perseveration and drawing evaluations were performed by means ofa Chi-squared metric (x2).

3. Results

3.1. Neuropsychological assessment

The statistical comparisons of the data obtained by the three experimental groups on the previously describedneuropsychological tests are shown in Table 2. As expected, PWS and WS individuals’ performances were significantly worsethan those of TD children on task assessing visuo-motor abilities (VMI). On tests assessing short term memory (VSS, VOS), nosignificant differences between PWS and TD children were found, while WS participants’ performances were significantlyworse than those of TD children on VSS task.

3.2. Multiple-reward explorative task

3.2.1. Search time

In all configurations PWS and WS individuals spent more time to complete the task than TD children (Fig. 1A). A two-wayANOVA (group� configuration) revealed a significant group effect (F2,38 = 21.22; P< .0001), while configuration effect(F2,76 = 2.2; P n.s.) and interaction (F4,76 = 1.36; P n.s.) were not significant. Post hoc comparisons on group effect revealedsignificant differences between pathological groups versus the TD children (PWS vs. WS: P< .05; PWS vs. TD: P< .001; WS vs.TD: P< .005).

3.2.2. Total errors

A two-way ANOVA (group� configuration) on total errors revealed significant group (F2,38 = 3.51; P< .05) andconfiguration (F2,76 = 13.44; P< .001) effects. Also the interaction was significant (F4,76 = 3.41; P< .05). As revealed by post

hoc comparisons on the interaction, in Cluster and Cross configurations the PWS individuals performed percentages of totalerrors significantly higher than the TD children, while in Matrix configuration the performances of both groups are similar.On the contrary, the WS participants performed significantly higher percentages of total errors than the TD children inMatrix configuration. No significant differences were found between PWS and WS participants’ performances in anyconfiguration (Fig. 1B).

3.2.3. Spatial span

The longest sequence of correct visits represented a measure of the spatial span (Fig. 1C). A two-way ANOVA (group xconfiguration) revealed significant group (F2,38 = 3.98; P< .05) and configuration (F2,76 = 12.67; P< .0001) effects. Also theinteraction was significant (F4,76 = 3.29; P< .05). Post hoc comparisons on interaction indicated that both syndromic groupsexhibited spatial span shorter than the TD participants in the Cross configuration.

able 2

tatistical comparisons of performances of PWS, WS and TD participants (one-way ANOVA and Duncan’s post hoc comparisons).

ognitive domain PWS

Mean

(�SEM)

WS

Mean

(�SEM)

TD

Mean

(�SEM)

Group effect

F(fd)

P

Post hoc

isuo-motor integration (VMI) 11.60

(�.56)

12.46

(�.66)

15.31

(�.55)

F(2,38) = 10.47,

= .00024PWS vs. WS n.s.

PWS vs. TD = .00019WS vs. TD = 0.002

isuo-spatial short-term memory (VSS) 3.37

(�.19)

2.23

(�.20)

3.38

(�.26)

F(2,38) = 8.68,

<.00079PWS vs. WS = .0009PWS vs. TD n.s.

WS vs. TD = .0011

isuo-object short-term memory (VOS) 2.69

(�.17)

2.46

(�.14)

2.77

(�.20)

F(2,38) = 78, n.s.

T

S

C

V

V

V

[(Fig._1)TD$FIG]

Fig. 1. Performances displayed by PWS, WS and TD participants on the search task in Cluster, Matrix and Cross configurations. Buckets arrangement in the

three configurations is depicted at the figurines below the graphs. The asterisks indicate the significance level of post hoc comparisons among groups

(*P< 05; ***P< 0005).

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107 101

3.2.4. Distance traveled

A two-way ANOVA (group� configuration) revealed a significant group (F2,38 = 3.3; P< .05) and configuration(F2,76 = 35.66; P< .001) effects. Interaction effect was not significant (F4,76 = 1.49; P n.s.). Post hoc comparisons on groupeffect indicated that the PWS individuals traveled distances not significantly different from the TD children, while the WSindividuals traveled distances significantly different from the TD children (P< .02) (Fig. 1D).

3.2.5. Error-free trials

Kruskal–Wallis test failed to reveal any significant difference among groups in the Cluster and Matrix configurations(Cluster: PWS = 18, WS = 14, TD = 18, H = .82, P n.s.; Matrix: PWS = 12, WS = 5, TD = 13, H = 3.50, P n.s.), while in the Crossconfiguration there was a significant difference among groups (Cross: PWS = 3, WS = 4, TD = 15, H = 10.89, P< .03. Mann–Whitney U test: PWS vs. TD: Z = 2.94, P< .005; WS vs. TD: Z =�2.46, P< .05; PWS vs. WS: Z = 0.29, P n.s.).

3.2.6. Perseverations

Chi-square analysis demonstrated that only the WS participants exhibited perseverative behaviors (PWS vs. WS: 20.95,P< .0001; PWS vs. TD: 20.95, P n.s.; WS vs. TD: 12.46, P< .0005).

3.2.7. Frequency of visits

To analyze if the number of visits to a given bucket was related to its spatial position, the frequency of visits to each bucketin each configuration was analyzed. In the Matrix configuration, a two-way ANOVA (group� bucket) revealed no significantgroup effect (F2,38 = 2.18; P n.s.), while a significant bucket effect (F8,304 = 7.89; P< .0001) was found. The interaction(F16,304 = 88; P n.s.) was not significant. Post hoc comparisons on the bucket revealed that the central bucket was visited lesstimes by all participants of all groups (at least P< .00001). In both Cluster and Cross configurations, the nine buckets wereequally visited, as indicated by two-way ANOVAs (group� bucket) (Cluster: group effect: F2,38 = 1.50, P n.s, bucket:F8,304 = 1.86, P n.s, interaction: F16,304 = 1.39; P n.s; Cross: group: F2,38 = 04, P n.s, bucket: F8,304 = 1.21, P n.s., interaction:F16,304 = 1.37; P n.s).

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107102

3.3. Search strategies in Cluster configuration

In a configuration displaying grouped rewards, such as the Cluster, subjects should complete each cluster before movingon to the next one. In this way, only three items at a time (the three buckets within a cluster) and the position of the threeclusters have to be remembered. We analyzed whether the participants used the spatial constraints afforded by the clusteredspace in this principled manner through additional parameters. One-way ANOVAs on the number of clusters visited revealedno difference among groups (F2,38 = .15; P n.s.). Also the number of clusters visited with three consecutive correct visits was notsignificantly different among groups (F2,38 = 1.02; P n.s.). By analyzing the kind of error, we found that PWS individuals werethe only participants who did not perform within-cluster errors (Fig. 2), as revealed by post hoc comparisons of the significantone-way ANOVA (F2,38 = 4.06; P< .05). All groups made a similar number of across-cluster errors (one-way ANOVA:F2,38 = 0.05; P n.s.).

3.4. Drawings

Almost all PWS, WS and TD participants willingly drew the spatial setting where they had just ‘‘played,’’ regardless ofgender and mental age. However, some TD children and a few WS participants drew figures or places not related with thespatial settings, and thus these pictures have not been considered in the drawing evaluation. The three spatial configurationswere represented consistently with their real organization by a number of participants limited and not significantly differentamong groups (Table 3A). Most PWS and TD participants were similarly accurate in drawing little elements of buckets, suchas the swinging covers or the little balls inside (Table 3B). Intriguingly, both syndromic groups exhibited a superiorcompetence in comparison to TD children when the cardinality (9� 1 buckets) was evaluated (Table 3C). A significantly highernumber of PWS drawings presented an excessive number of elements (‘‘hyper-cardinality’’) (Table 3D), while a significantlyhigher number of TD drawings presented a low number of elements (‘‘hypo-cardinality’’) (Table 3E). Finally, no drawing of PWSindividuals was characterized by an egocentric vision in which the subject represented him/herself within the setting. Conversely,the egocentric representation was present in some TD drawings (Table 3F).

4. Discussion

In the present research we have analyzed how the characteristics of an environment affect the explorative abilities inPWS individuals. To this aim we evaluated their performances in a large-scale task with multiple rewards and comparedthem with those of mental age- and gender- matched TD children. Moreover, we evaluated also another syndromic groupcomposed by WS individuals to determine whether the performance pattern exhibited by PWS participants was specific tothis population or whether it was due to a non-specific effect of intellectual disability.

The PWS individuals exhibited different performances according to the type of spatial configuration explored. In theCluster configuration, they spent more time, made more errors and tended to travel more distance in comparison to TDchildren, as revealed by their explorative patterns (Fig. 3). An analogous but not identical pattern was observed in the Crossconfiguration where they also exhibited lower values of span. On the contrary, in the Matrix configuration the performancesof PWS and TD participants were similar. Furthermore, as TD children, PWS individuals did not display tendencies toperseverate (consecutively re-exploring the same buckets).

To explain the exploratory behavior of the PWS participants and their processing of spatial information, it is important totake into account the characteristics of the three configurations.

[(Fig._2)TD$FIG]

Fig. 2. Performances displayed by PWS, WS and TD participants in Cluster configuration. The asterisk indicates the significance level of the one-way analyses

of variance (*P< 05).

Table 3

Evaluation of graphic and mental representative mapping abilities of PWS, WS and TD participant.

Featuresa Total drawings Chi-squared test

PWS WS TD

[TD$INLINE]

11 7 6

PWS vs. WS: .34 n.s.

PWS vs. TD: .71 n.s.

WS vs. TD: .07 n.s.

[TD$INLINE]

27 10 24

PWS vs. WS: 4.012<.05PWS vs. TD: .005 n.s.

WS vs. TD: 4.078<.05

[TD$INLINE]

18 17 2

PWS vs. WS: .05 n.s.

PWS vs. TD: 8.98<.005WS vs. TD: 9.76<.005

[TD$INLINE]

9 9 22

PWS vs. WS: 2.68 n.s.

PWS vs. TD: 7.23<.05WS vs. TD:1.42 n.s.

[TD$INLINE]

18 7 33

PWS vs. WS: .08 n.s.

PWS vs. TD: 5.47<.05WS vs. TD: 3.96<.05

[TD$INLINE]

0 2 10

PWS vs. WS: 2.25 n.s.

PWS vs. TD: 10.28<.005WS vs. TD: 4.66<.05

a All drawings are made by PWS participants, but the last one made by a TD child.

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107 103

An environment organized in clusters allows to be explored with the possibility of chunking it, first visiting the locationswithin the same cluster and then moving to another one. The ‘‘chunking theory’’ predicts that once the chunks have beenexplored the burden on memory should be lightened from the total number of buckets to be explored (in our case, nine) tothe number of clusters constituting the search space (in our case, three) (Foti et al., 2007, 2010; Foti, Petrosini, et al., 2011).Thus, the hierarchical organization of memory afforded by chunking substantially reduces the working memory load andpromotes higher level performances (Terrace & McGonigle, 1994). Despite suitable to be simplified, the Cluster configurationresulted to be difficult for PWS individuals suggesting that they rarely used a chunking procedure. The lack of workingmemory errors exhibited by the PWS participants further supports the hypothesis of their procedural deficit (Fig. 2). In theCluster configuration the PWS performances were fully consistent with those displayed by others PWS individuals in a radialmaze task, in which they exhibited impaired performances on the parameters more specifically linked to explorative

[(Fig._3)TD$FIG]

Fig. 3. Explorative trajectories of PWS, WS and TD participants in exploring the Cluster, Matrix and Cross configurations. The trajectories traveled by all

individuals of each group in the first and second trial of the task are reported.

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107104

strategies. Namely, the PWS participants exhibited reduced use of a chaining strategy, as indicated by low percentage ofconsecutively entering string of adjacent arms (Foti, Menghini, et al., 2011).

Efficient strategies for exploring the Matrix configuration are structured search patterns that follow rows (or columns)sequentially or, conversely, that travel the perimeter of the external ‘‘square’’ to reach the most internal bucket at the end.When the strategic use of these searching patterns is loosened, a compromise between an explorative behavior promoting anextended search among rewarded buckets (i.e., visiting buckets farther away than those previously visited or followingdiagonal trajectories between buckets) and a behavior that limits the information to be stored (i.e., visiting the nearestbucket) may be used (Foti et al., 2007, 2010; Foti, Petrosini, et al., 2011).

The PWS individuals exhibited a number of total errors not significantly different from TD children, although theytook twice the time to explore the setting, indicating that when the environment is shaped up according to theexplorative abilities of the subject, procedural deficits can be by-passed (Mandolesi, Leggio, Spirito, & Petrosini, 2003).This interpretation is consistent with the hypothesis that spatial information processing is dependent on, or stronglyrelated to, the structural affordances of the search space and it explains why the PWS performances are reported to beexcellent in some spatial tasks (Dykens, Hodapp, Walsh, & Nash, 1992; Verdine et al., 2008) but impaired in others(Woodcock et al., 2009). Thus, the PWS performance in a given spatial task seems to be determined by the proceduralload it requires.

Cross configuration is characterized by strong spatial constraints. The trajectory adopted to explore a cross can work as anotational system that aids the use of a principled pattern and reduces the memory load, at least in the exploration of the firstline once a firm directional principle preventing the inversion of the travel direction is applied. The most efficient strategy tofully deplete the cross requires that the subject uses an end-to-end search pattern twice, moving along the lines and visitingthe near buckets. However, once a line is depleted and the subject reaches the end of the first line, it is necessary to changeline (and thus strategy) to reach the farthest buckets. Traveling on, the subject re-encounters the central bucket that can becorrectly skipped only in the case of an already formed cognitive spatial map and of effective working memory functions.Thus, the exploration of the Cross configuration is a challenging task that requires both procedural (change of strategy) andmnesic (memory load) components (Foti et al., 2007, 2010; Foti, Petrosini, et al., 2011). The PWS participants obtainedperformances worse in comparison to the TD children. In particular, they took more time, made more total errors andobtained lower span values. Although this response pattern could result from both procedural and mnesic deficits, the notimpaired performances of the PWS participants on tests assessing short-term memory (VSS, VOS; Table 2) once againsuggest the procedural nature of their deficit. Thus, the structural affordances of the environment do influence theexploration and determine how spatial information is processed.

The comparison between syndromic groups revealed similar difficulties in exploring the Cross configuration but mirroredpattern of response in the other configurations. Thus, both syndromic groups exhibited some spatial deficits conveyedaccording to the spatial affordances of the environment.

For a successful spatial exploration it is necessary that the different cerebral systems cooperate with each other (Lehnunget al., 2003; Etienne & Jeffery, 2004). Namely, the knowledge of the environment by exploring/walkway in it appears to bemainly linked to the proper functioning of the fronto-parietal cortical networks and some sub-cortical structures, such ascerebellum and basal ganglia and to their bidirectional interconnections with cortical circuitries (Foti, Menghini, et al., 2011).While the brain abnormalities of WS individuals have been well described (Atkinson et al., 2006; Tomaiuolo et al., 2002), onlyfew studies documented the brain abnormalities in PWS subjects. In particular, neuro-pathological anomalies in cerebellar

F. Foti et al. / Research in Developmental Disabilities 38 (2015) 97–107 105

and fronto-parietal structures (Hayashi et al., 1992; Woodcock et al., 2010), decreased volume of the parietal-occipital lobe(Miller et al., 2007), reduced gray-matter volume in the orbito-frontal cortex, caudate nucleus, inferior temporal gyrus,precentral gyrus, supplementary motor area, postcentral gyrus, and cerebellum (Ogura et al., 2011) have been described.These neuro-anatomical abnormalities may be the structural basis of the spatial procedural deficit of the PWS participantsobserved in the present research, since the dysfunction of fronto-parietal circuit as well as the alterations of sub-corticalstructures are retained to be closely related to impaired spatial strategies (Foti, Menghini, et al., 2011; Foti, Petrosini, et al.,2011).

The procedural deficit exhibited by the PWS individuals could also affect the development of their spatial declarativeknowledge, since altered explorative strategies make the acquisition of the spatial cognitive map extremely demanding(Mandolesi et al., 2003). It is accepted that a subject not able to appropriately explore an environment will not be able torepresent it. The analysis of mapping abilities performed through the drawings of the participants provided anindication of the spatial declarative knowledge in PWS individuals. In most PWS drawings, the shape of the spatialconfigurations was not correctly represented (Table 3A), although many minute details were drawn (Table 3B). Even theTD children (of about 6 years of age) were unable to represent the shape of the spatial settings, consistently with theevidence that the hippocampal structures related to the spatial declarative knowledge fully mature at about 10 years ofage (Klingberg, 2006; Lehnung et al., 1998; Mandolesi, Petrosini, et al., 2009; Pine et al., 2002). Interestingly, PWSparticipants, as WS individuals, exhibited superior abilities in representing the correct number of elements of the threespatial configurations in comparison to TD children (Table 3C). Thus, despite some impairments in spatial mapping, thePWS individuals exhibited a function of cardinality above the level exhibited by the mental age-matched TD children.Notably, the chronological ages of the PWS participants were much higher than those of the mental age-matched TDchildren. Thus, a possible explanation for this unexpected skill of PWS individuals could be related to their longerexperience with rote counting. In fact, the ability to rote count and to use counting to determine the total numerosity ofa set is a basic numerical ability that all individuals repeatedly practice in their daily lives. Another intriguing feature ofthe PWS drawings was the tendency to reproduce a very high number of setting elements (more than 70 buckets!) notshared with any other participant (Table 3D). The PWS tendency to the hyper-cardinality could be related with theircompulsive and ritualistic behaviors well described in literature (Clarke, Boer, Chung, Sturmey, & Webb, 1996; Copetet al., 2010; Dimitropoulos, Blackford, Walden, & Thompson, 2006; Dykens, Leckman, & Cassidy, 1996; Holland et al.,2003).

5. Conclusions

In conclusion, the present study evidenced the impairment of explorative functions in the PWS individuals. In particular,their deficit appeared to be related to compromised spatial procedural components that were overcome when the structuralaffordances of the environment allowed it. In these favoring conditions the PWS performances became in line with those ofTD children.

The present findings suggest that for an optimally explore the daily environment, it should be modified in accordance tothe specific explorative abilities of ID individuals. In the case of PWS, each element of the environment should maintainsequential features with the previous and the next element, without creating spaces too dispersed. In practical terms, thisinformation could be put into effect with the construction of daily environments in which the path to follow is sequentiallymarked, as a signed mountain trail.

Being able to explore the environment allows interacting with the elements within it, stimulating spatial knowledge,increasing the orientation, and indirectly improving cognitive functions. In addition, the ability to move into an environmentpermits to interact actively with others, increasing the socialization. Creating an environment appropriate to their ownexploration abilities leads the ID individuals toward the conquest of autonomy.

Acknowledgements

This work was supported by Foundation Jerome Lejeune grants to L.M. We would like to thank C. Rufini for her kind helpin testing some children. We would also like to thank the children with Prader–Willi and Williams syndromes and theirparents for making this study possible.

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