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Learning by Observation: Insights from Williams Syndrome
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  Learning by Observation: Insights from WilliamsSyndrome Francesca Foti 1,2 * . , Deny Menghini 3 . , Laura Mandolesi 4,2 , Francesca Federico 1 , Stefano Vicari 3 ,Laura Petrosini 5,2 1 Department of Developmental and Social Psychology, University ‘‘Sapienza’’ of Rome, Rome, Italy,  2 IRCCS Santa Lucia Foundation, Rome, Rome, Italy,  3 ChildNeuropsychiatry Unit, Neuroscience Department, ‘‘Children’s Hospital Bambino Gesu’’’, Rome, Rome, Italy,  4 School of Movement Sciences (DiSIST), University of Naples‘‘Parthenope’’, Naples, Italy,  5 Department of Psychology, University ‘‘Sapienza’’ of Rome, Rome, Italy Abstract Observing another person performing a complex action accelerates the observer’s acquisition of the same action and limitsthe time-consuming process of learning by trial and error. Observational learning makes an interesting and potentiallyimportant topic in the developmental domain, especially when disorders are considered. The implications of studies aimedat clarifying whether and how this form of learning is spared by pathology are manifold. We focused on a specificpopulation with learning and intellectual disabilities, the individuals with Williams syndrome. The performance of twenty-eight individuals with Williams syndrome was compared with that of mental age- and gender-matched thirty-two typicallydeveloping children on tasks of learning of a visuo-motor sequence by observation or by trial and error. Regardless of thelearning modality, acquiring the correct sequence involved three main phases: a detection phase, in which participantsdiscovered the correct sequence and learned how to perform the task; an exercise phase, in which they reproduced thesequence until performance was error-free; an automatization phase, in which by repeating the error-free sequence theybecame accurate and speedy. Participants with Williams syndrome beneficiated of observational training (in which theyobserved an actor detecting the visuo-motor sequence) in the detection phase, while they performed worse than typicallydeveloping children in the exercise and automatization phases. Thus, by exploiting competencies learned by observation,individuals with Williams syndrome detected the visuo-motor sequence, putting into action the appropriate proceduralstrategies. Conversely, their impaired performances in the exercise phases appeared linked to impaired spatial workingmemory, while their deficits in automatization phases to deficits in processes increasing efficiency and speed of theresponse. Overall, observational experience was advantageous for acquiring competencies, since it primed subjects’ interestin the actions to be performed and functioned as a catalyst for executed action. Citation:  Foti F, Menghini D, Mandolesi L, Federico F, Vicari S, et al. (2013) Learning by Observation: Insights from Williams Syndrome. PLoS ONE 8(1): e53782.doi:10.1371/journal.pone.0053782 Editor:  Tricia A. Thornton-Wells, Vanderbilt University, United States of America Received  July 12, 2012;  Accepted  December 4, 2012;  Published  January 10, 2013 Copyright:  2013 Foti et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricteduse, distribution, and reproduction in any medium, provided the srcinal author and source are credited. Funding:  This work was supported by the Fondation Je´roˆme Lejeune to L.M. The funders had no role in study design, data collection and analysis, decision topublish, or preparation of the manuscript. Competing Interests:  The authors have declared that no competing interests exist.* E-mail: francesca.foti@uniroma1.it .  These authors contributed equally to this work. Introduction In humans and other animals new competencies may be learnedthrough active experience and through observation of others’experience [1,2]. Observing another person performing a complexaction accelerates the observer’s acquisition of the same action andlimits the time-consuming process of learning by trial and error[3–5]. Indeed, observational learning does not just involve copying an action and requires that the observer transforms theobservation into an action as similar as possible to the model interms of the goal to be reached and the motor strategies to beapplied [5–10].Observational learning is already present at birth [5,11–13] andit is crucial for developing complex abilities such as language,social responsiveness, use of instruments to get things done [9,14].Thus, in children, learning new competencies by observing adultsor peers is a central process in cognitive development [15].By using an innovative task based on learning to detect a visuo-motor sequence, we demonstrated that in the presence of dyslexiathe ability to learn by observation a previously observed visuo-motor sequence was markedly impaired, while the ability to detecta correct sequence by trial and error was preserved [16]. In thepresent research we focused on a population with learning as wellas intellectual disability (ID), the Williams syndrome (WS) whosewell-known neuropsychological profile with specific points of strengths and weaknesses allowed singling out cognitive processesworking as learning went by. WS individuals show severelyimpaired visuo-spatial processing, planning and implicit learning [17–22], while they exhibit relatively preserved perception of the visual characteristics of objects and face recognition [23]. WSindividuals have specific difficulty in maintaining visuo-spatialinformation in working memory and in performing long-termmemory tasks [24,25], consistently with a deficit of dorsal stream.Considering that the visuo-motor task to be learned by observationrequired to translate visual information into action, specific PLOS ONE | www.plosone.org 1 January 2013 | Volume 8 | Issue 1 | e53782  function of dorsal stream network [26,27], WS individuals appearto be the ideal participants to investigate the cognitive processesinvolved in the observational learning. Performances of a group of WS individuals were compared with those of a mental age- andgender-matched group of typically developing (TD) children on atask requiring the learning of a visuo-motor sequence. Theparticipants learned the sequence either by performing the task after observing an actor detect the sequence of correct items bytrial and error (observational training) or by actually performing the task by trial and error (Fig. 1). Materials and Methods Participants Twenty-eight WS participants and 32 TD children (used ascontrols) matching the WS individuals for mental age (MA) havebeen examined in the present study constituted by two experi-mental conditions: Learning by Trial and Error followed byObservational Learning (Condition 1); Observational Learning followed by Learning by Trial and Error (Condition 2) (Table 1).Only WS individuals with mental age (MA) of at least 5 years wereincluded in the present research because participants with inferiorMA did not succeed in completing the task. No significantdifferences in chronological age (CA), MA and IQ (  P   always . 0.2)among participants performing Conditions 1 and 2 were found(Table 2).The clinical diagnosis of WS was confirmed by fluorescence  insitu  hybridization (FISH) genetic investigation, which showed thecharacteristic deletion on chromosome band 7q11.23. WSparticipants were part of a larger pool of individuals with learning disabilities attending the Children’s Hospital Bambino Gesu` of Rome for clinical and rehabilitative follow-up. All of them lived athome with their families. The parents of all individuals whoparticipated in the study provided written informed consent. Thisstudy was approved by the Ethic Committee of the Children’sHospital Bambino Gesu` of Rome and conducted according to theHelsinki declaration.WS individuals were tested in a quiet room at the Children’sHospital Bambino Gesu`. TD children were individually tested in aquiet room at their schools. Intelligence Evaluation and NeuropsychologicalAssessment In the present study, the brief version of the Leiter InternationalPerformance Scale–Revised [28] was employed (four out of 10subtests: Figure Ground, Form Completion, Sequential Order andRepeated Patterns). The brief IQ and the corresponding mentalages were computed. Visuo-motor integration [29], visuo-spatialperception [30] and memory [31] were assessed (Table 3). Experimental Procedure Each participant was sat in front of a computer touch screen(distance 60 cm). In both Conditions, the experimenter acting as Figure 1. Schematic diagrams of the two experimental conditions.  Condition 1: Learning by Trial and Error followed by ObservationalLearning: participants detected a sequence by trial and error (TE1), then they observed an actor detecting a sequence different from the one they hadpreviously detected (observational training) and, finally, they reproduced the observed sequence (OBS2). Condition 2: Observational Learningfollowed by Learning by Trial and Error: participants were submitted to an observational training, then they reproduced the observed sequence(OBS1) and, finally, detected by trial and error a different sequence they had never observed (TE2). The incorrect positions touched by the actorduring the observational training are evidenced in grey. S: starting point; F: final point.doi:10.1371/journal.pone.0053782.g001Learning by Observation in Williams SyndromePLOS ONE | www.plosone.org 2 January 2013 | Volume 8 | Issue 1 | e53782  the actor (F.F.) was sat near the participant. A 8 6 8 black matrixappeared on the touch screen. The subject was asked to find ahidden sequence of ‘‘correct’’ squares prepared in advance by theexperimenters. The sequence was composed of 10 adjacent spatialpositions in the matrix, which formed a ‘‘snake-like’’ pattern(Fig.1). To explain the task to each participant the experimenterused the same verbal instructions: ‘‘You have to find a routeformed by ten squares. When you touch a correct square it will beturned grey and you will hear a sound; conversely, if you touch awrong square, it will be turned red. In this case, you have to find anew grey square. You have to start the route each time you find anew correct square. After finding the whole route, you have to re-touch it three times without making lighted red squares’’. Theparticipants started touching a grey square, which was the firstelement of the sequence and was always lit up. In the search forthe second correct square, the participants had to touch one of thefour squares bordering the grey square by moving in the matrix vertically or horizontally, but never diagonally. Each touchedsquare (correct or incorrect) was lit up for 500 ms and then lightedoff again; thus, no trace of the performed sequence remained onthe screen. In learning the sequence by trial and error, theparticipants tried to find the correct sequence immediately afterthe verbal instructions. Conversely, in the observational learning task after the verbal instructions the participants observed theexperimenter while she detected a 10-item sequence by trial anderror (observational training). The experimenter performed thetask by always making the same errors in the same positions, sothat all participants observed the same pattern of correct andincorrect touches. Two minutes after the end of the observationaltraining the participants were required to actually reproduce theobserved correct sequence.The tasks involved three phases: the Detection Phase (DP) thatended once the participants found the tenth correct position; theExercise Phase (EP) in which they had to repeat the 10-itemsequence until their performance was error-free; the Automatiza-tion Phase (AP) that ended when the correct sequence wasrepeated three consecutive times without errors. Parameters Error parameters:  DP errors,  calculated as the number of incorrect items touched in detecting the ten correct positions;  EP repetitions,  calculated as the number of replications needed to reachthe error-free performance. Time parameters:  AP times   (in msec),calculated as the time spent carrying out each of the threerepetitions of the sequence. Analysis of Error To assess the kind of error further parameters were taken intoaccount considering the two phases DP and EP together: thenumber of   sequence errors  , as touching a ‘‘correct’’ square in‘‘wrong’’ moment (e.g. touching E7 before than F7);  side-by-side errors  , as touching the squares bordering the ‘‘correct’’ sequence(e.g. E8);  illogical errors  , as touching any other square (e.g. B5); Table 1.  Description of WS groups (WS1 and WS2) and TD groups (TD1 and TD2) performing the two different experimentalconditions. Condition 1: Learning by Trial and Error followed by Observational LearningGroup Number GenderCAMean  ±  SEMMAMean ±  SEMIQMean  ± SEM WS1 14 9 M 19.83 6 1.42 6.52 6 0.16 54.87 6 1.69TD1 16 11 M 6.78 6 0.15 7.02 6 0.28 106.12 6 2.51 Condition 2: Learning by Observation followed by Learning by Trial and Error WS2 14 8 M 17.64 6 1.37 6.60 6 0.19 53.68 6 1.36TD2 16 8 M 6.76 6 0.11 7.40 6 0.28 111.62 6 2.06CA: Chronological Age.MA: Mental Age.IQ: Intelligence Quotient.doi:10.1371/journal.pone.0053782.t001 Table 2.  Comparisons of chronological age (CA), mental age (MA) and Intelligence Quotient (IQ) between WS groups (WS1 andWS2) and TD groups (TD1 and TD2) that performed the two different experimental conditions. GroupCAMean ±  SEM F (freedom degrees)MAMean  ± SEM F (freedom degrees)IQMean ±  SEM F (freedom degrees) WS1 19.83 6 1.42 (1,26)0.61 P=0.43 6.52 6 0.16 (1,26)0.04 P=0.83 54.87 6 1.69 (1,26)0.15 P=0.70 WS2 17.64 6 1.37 6.60 6 0.19 53.68 6 1.36TD1 6.78 6 0.15 (1,30)0.005 P=0.94 7.02 6 0.28 (1,30)0.45 P=0.50 106.12 6 2.51 (1,30)1.43 P=0.23 TD2 6.76 6 0.11 7.40 6 0.28 111.62 6 2.06doi:10.1371/journal.pone.0053782.t002 Learning by Observation in Williams SyndromePLOS ONE | www.plosone.org 3 January 2013 | Volume 8 | Issue 1 | e53782   perseverations,  as consecutively touching the same item or a fixedsequence of items. Furthermore, in the task of observationallearning we calculated the number of   imitative errors  , as touching thesame squares wrongly touched by the actor during the observa-tional training (e.g. F4) (Fig.1). Condition 1: Learning by Trial and Error Followed byObservational Learning Fourteen WS and 16 TD individuals (Table 1) firstly detected asequence by Trial and Error (TE1) and, after ten minutes fromtask end, they were submitted to the observational training. Aftertwo minutes, participants were required to actually reproduce theobserved sequence (OBS2). There was no fixed time limit forexecuting the task. A pilot study was conducted to verify if the two sequencesarranged to be used as ‘‘TE’’ and ‘‘OBS’’ sequences did not differas to degree of difficulty. Six TD children [3 M] of mental age6.10 6 0.3 detected the two different sequences by trial and error;presentation order was randomized among participants. Errorsmade in detecting each sequence were calculated by one-way ANOVA with repeated measures. The analysis failed to reveal anysignificant difference between sequences (  F  (1,5) =0.63,  P  =0.46),confirming sequences of the same difficulty. Condition 2: Learning by Observation Followed byLearning by Trial and Error Fourteen WS and 16 TD individuals (Table 1) first observed theexperimenter detect a sequence (OBS1) and then actuallyreproduce it. After ten minutes from task end, they detected adifferent sequence by trial and error (TE2). Thus, the difference of the two conditions was that participants reproduced a sequencelearned by observation  after   (Condition 1) or  before   (Condition 2) thedetection of a different sequence by trial and error.To evaluate mental representative mapping abilities, at the endof the reproduction of the sequence participants were required todraw the arrangement of the sequence on a 8 6 8 matrix sketchedon a paper sheet. Thus, any participant drew the arrangement of two sequences, one learned by observation and the other one bytrial and error. Mapping abilities were evaluated by tabulating the variable ‘‘errors’’ into three categories: ‘‘no error’’, ‘‘one error’’and ‘‘more than one error’’. Attentional Task  The sustained attentional abilities of all participants were tested.Participants sat in front of a computer monitor and were requiredto put their left index fingers on the A key of the keyboard and toput their right index fingers on the L key. The visual stimulus wasa grey circle presented on monitor center for a duration varying from 1400 (short) to 2600 (long) msec in steps of 200 msec in arandomized order. Participants were submitted to a brief training in which they were instructed to judge 20 stimuli as short or long and to press the A or L keys, respectively. In the testing phase theparticipants had to judge the duration of 70 stimuli (10 stimuli of each of the 7 durations) and to press the A or L keys as quickly aspossible after the stimulus appeared. The computer programrecorded reaction times (with 1-ms resolution) and accuracy of theresponse. The responses were then analyzed by clustering them inblocks of ten (regardless of stimulus duration) (i.e. 1–10, 11–20,21–30….61–70). Statistical Analyses The data were first tested for normality (Shapiro-Wilk normalitytest) and homoscedasticity (Levene test) and then compared byusing two-way, three-way or four-way analyses of variance(ANOVAs). The two-way ANOVAs were performed by applying the mixed model for independent variable (group) and repeatedmeasures (error, square or block). Three-way ANOVAs (group 6 condition 6 task) were performed on most parameters, while thefour-way ANOVA on the three AP times was performed byapplying the mixed model for independent variables (group,condition and task) and repeated measures (time). These analyseswere followed by post-hoc multiple comparisons using Newman– Keuls test. In evaluating mapping abilities the error categorieswere analyzed by Chi-Square.Because the 28 WS participants were differently aged (N=9 agerange: 8;9–14;1; N=10 age range: 14;9–19;9; N=9 age range:22;9–35;3), we verified the sample homogeneity by comparing theperformances of three differently aged WS sub-groups on threemain parameters of the learning tasks they performed (DP errors;EP repetitions and AP times) by using MANOVAs. These analysesrevealed no significant difference among WS sub-groups’ perfor-mances. Namely, in the tasks of learning by trial and error (TE1– TE2), the MANOVA revealed a not significant sub-group effect(F (2,25) =0.12,  P  =0.88) and a significant parameter effect Table 3.  Statistical comparison of visuo-spatial performances of WS and TD participants. WSMean ±  SEMTDMean ±  SEM Effect F (1, 58)  value  P  Visuo-motor integration 13.39 6 0.50 15.25 6 0.26 Group 11.37 0.0013Visuo-spatial short-term memory (VSS) 2.79 6 0.20 3.53 6 0.14 GroupTask Interaction8.299.634.820.00550.00290.032Newman–Keuls testVSS: 0.00021VOS: 0.36Visuo-object short-term memory (VOS) 2.64 6 0.12 2.91 6 0.11Visuo-perception test – Spatial (VPT-S) 15.18 6 1.07 18.03 6 .77 GroupTask Interaction7.0665.754.060.010 , 0.00010.048Newman–Keuls testVPT-S: 0.00038VPT-F: 0.31Visuo-perception test – Form (VPT-F) 11.32 6 0.36 12.16 6 0.26doi:10.1371/journal.pone.0053782.t003 Learning by Observation in Williams SyndromePLOS ONE | www.plosone.org 4 January 2013 | Volume 8 | Issue 1 | e53782  (F (2,50) =154.54,  P  , 0.0001). The interaction was not significant(F (4,50) =0.13,  P  =0.96). In the tasks of observational learning (OBS1–OBS2) the MANOVA also revealed a not significant sub-group effect (F (2,25) =0.47,  P  =0.62) and a significant parametereffect (F (2,50)= 85.46,  P  , 0.0001). The interaction was not signif-icant (F (4,50) =0.47,  P  =0.75). Thus, we pooled together the 28differently aged WS individuals. All statistical analyses were performed by using Statistica 8.0 forWindows and the significance level was established at  P  , 0.05. Results Learning Tasks WS participants performed a number of DP errors notsignificantly different from TD children after the observationaltrainings (OBS1–OBS2) and were significantly impaired indetecting the sequence by trial and error in TE1 compared withany other intra- or inter-group condition (Fig. 2A), as revealed bypost-hoc comparisons (always  P  , 0.001) on the second-orderinteraction (F (1,56) =8.37,  P = 0.0054) of the three-way ANOVA(group 6 condition 6 task).In EP, when individuals repeated the sequence until theirperformance was error-free, WS participants needed a significant-ly higher number of repetitions in comparison to TD childrenregardless of condition (1 or 2) and trial (OBS or TE), as revealedby the group effect (F (1,56) =9.58,  P  =0.0030) of the three-way ANOVA (Fig. 2B). The analysis of the three AP times revealedthat although all participants exhibited significantly reduced timesas the task went by (F (2,112) =27.62,  P  , 0.00001), WS individualswere significantly slower than TD children (F (1,56) =10.37, P  =0.0021), revealing a difficulty in automatizing the sequence(Fig. 2C). Analysis of Error In TE1, although WS and TD participants did not differ inthe number of illogical errors, WS individuals exhibited valuesof sequence, side-by-side and perseverative errors higher thanTD children, as revealed by post-hoc comparisons made on theinteraction (F (3,84) =3.14,  P  =0.029) of the two-way ANOVA(group 6 kind of error) (Fig. 3). The highest number of sequenceerrors of WS individuals was found in E7 and F7 squares whena change of strategy was required (i.e. after an error re-starting the sequence from the first item rather than continuing along on the ‘‘snake’’) (Fig. 1), as revealed by post-hoc comparisonsmade on the interaction (F (9,252) =1.96,  P  =0.044) of the two-way ANOVA (group 6 square) (Fig. 4). As for side-by-side errors,the high number of errors of WS individuals was due to theirsignificantly more frequent touching of a wrong square when achange of direction was required (squares: D7, F6, E1) (Fig. 1),as revealed by post-hoc comparisons made on the interaction(F (27,756) =2.42,  P  , 0.0001) of the two-way ANOVA (group 6 square) (Fig. 4).The analysis of error in the remaining tasks (OBS2, OBS1 andTE2) revealed no significant difference between groups, even if significant difference among kind of errors was found (always P  , 0.00001) (Fig. 3). Mapping Abilities Mental representative mapping abilities of the participants wereevaluated by having them draw the arrangement of sequences theyhad just performed. No significant difference among categories of errors and between groups was found in any sequence (  P   at least . 0.4). Attentional Task  Two-way ANOVAs (group 6 block) on reaction times orresponse accuracy of the WS and TD groups revealed noattentional decay in both groups, as indicated by not significantdifference in the reaction times in the seven blocks (F (6,348) =1.55, P  =0.15). A similar result was obtained when response accuracywas analyzed (F (6,348) =1.80,  P  =0.10). Notably, a significantdifference was found between WS and TD groups on reactiontimes (F (1,58) =13.52,  P  =0.00051), given WS participants pressedthe keys at the appearance of the stimulus more quickly than TDchildren (Fig. 5). Discussion Our study adopted a matched-group design to determinewhether the learning performance of WS individuals was above orbelow that expected given their general level of intellectualfunctioning indexed as MA. However, although this design is onethe most commonly employed measures of matching in IDresearch, we are aware that it has limitations in respect to ID-matched control group design that takes into account the cognitiveprofile of the specific pathology. Nevertheless, even the ID-matched control group cannot be taken as a guarantee of normative group, due cognitive profiles among different etiologicalgroups with ID exhibit different peaks and troughs [32]. In anattempt to overcome the difficulties in matching individuals of different groups on any one particular measure it has beenproposed the use of regression techniques that take the factorsrelated to task performance into account [32]. However, thismeasure requires specific statistical properties of the data (ashomogeneity of regression slopes or sample size), hardly availablein studies on population affected by rare genetic conditions as WS.The present study documented as WS participants significantlybeneficiated of observational training as TD MA-matchedchildren. This was true specifically in the DPs of learning tasks,while as for EPs and APs, in all tasks regardless of presentationorder (1 or 2) or learning modalities (OBS or TE), WS participantsperformed significantly worse than TD children. The powerfullypositive effect of observational training was present not only inreproducing the previously observed sequences (OBS1 and OBS2)but also affected the subsequent detection of a sequence by trialand error (TE2). However, the practice effect, inevitably present inany second task, potentially could affect performances.Since WS individuals exhibit difficulties in maintaining visuo-spatial information in working memory and in performing spatiallong-term memory tasks (Table 3) [20,24,25], their heavilyimpaired performances in all EPs appear linked to spatial working memory deficits and difficulties in bringing together the shortsequences detected during DP, in maintaining them in working memory to recall the whole sequence trace and in monitoring thecorrect execution of the sequence. These findings indicate that theobservational training exerts beneficial effects mainly on theacquisition of strategies to be applied.In both Conditions, WS participants displayed AP times longerthan TD children, even if progressively diminishing as the task went by. This finding was not a consequence of the fine motordeficits usually reported in WS individuals. In fact, consistentlywith Vicari et al. (2007) [22], the reaction times exhibited by WSgroup in the Attentional Task were even shorter than those of TDgroup. Thus, the longer WS times were related to deficits inautomatization processes increasing efficiency and speed of theresponse to reach highest levels of performance [33]. Automatizing skills is mainly linked to the functions of sub-cortical structures, asthe cerebellum and basal ganglia and to their bidirectional Learning by Observation in Williams SyndromePLOS ONE | www.plosone.org 5 January 2013 | Volume 8 | Issue 1 | e53782
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