PAPER

Human newborns match tongue protrusion of disembodiedhuman and robotic mouths

Robert Soussignan,1 Alexis Courtial,2 Pierre Canet,2 Gisele Danon-Apter3

and Jacqueline Nadel2

1. Centre des Sciences du Go�t et de l’Alimentation, Dijon, France2. Centre Emotion, H�pital de la SalpÞtri�re, Paris, France3. Unit� de Psychiatrie P�rinatale, Maternit� Ambroise Par�, Bourg-La-Reine, France

Abstract

No evidence had been provided so far of newborns’ capacity to give a matching response to 2D stimuli. We report evidence from18 newborns who were presented with three types of stimuli on a 2D screen. The stimuli were video-recorded displays of tongueprotrusion shown by: (a) a human face, (b) a human tongue from a disembodied mouth, and (c) an artificial tongue from arobotic mouth. Compared to a baseline condition, neonates increased significantly their tongue protrusion when seeingdisembodied human and artificial tongue movements, but not when seeing a 2D full-face protruding tongue. This result wasinterpreted as revealing the exploration of top-heavy patterns of the 2D face that distracted infants’ attention from the tongue.Results also showed progressively more accurate matching (full tongue protrusion) throughout repeated exposure to each kindof stimulus. Such findings are not in line with the predictions of the innate releasing mechanism (IRM) model or of the oralexploration hypothesis. They support the active intermodal mapping (AIM) hypothesis that emphasizes not only the importanceof repeated experience, as would the associative sequence learning (ASL) hypothesis, but also predicts a differential learningand progressive correction of the response adapted to each stimulus.

Introduction

Imitation has recently gained increasing interdisciplinaryattention as cognitive neuroscience has focused on thebrain coupling of perception and execution of action.Such a focus reactivates the debate around the theoreticalinterpretation of the neonatal capacity to match seen fa-cial movements. Meltzoff and Moore (1977), followingless well-known research by Zazzo (1957) and by Maratos(1973), demonstrated neonatal matching in a series ofcareful studies. In these studies, coders of newborns’recordings were blind to what the newborn actually saw,and researchers compared the frequencies of tongueprotrusion, mouth opening, lip protrusion or fingermovement, in two conditions: with and without the per-ception of a model performing the movement. Althoughreplication studies were not all conclusive, most resultsconfirmed the phenomenon (Abravanel & DeYong, 1991;Fontaine, 1984; Heimann & Schaller, 1985; Heimann,Nelson & Schaller, 1989; Kugiumutzakis, 1985; Legerstee,1991; Meltzoff & Moore, 1983, 1989; Nagy, Compagne,Orvos, Pal, Molnar, Jansky, Loveland & Bardo, 2005;Reissland, 1988; Vinter, 1986). Conditions required forsuccessful matching were analyzed.

In a meta-analysis of 23 experiments, Anisfeld (1991)stressed the role of demonstration duration on tongueprotrusion production: 5 ⁄ 16 studies obtained a tongueprotrusion effect for a total demonstration duration of40 sec or less, while a matching effect was obtained in7 ⁄ 7 studies when the minimum total demonstration was60 sec. Other methodological heterogeneity betweenstudies, including distance from the model, rhythm offacial movements and age of participants (from one hourafter birth up to 14 weeks), may contribute to thedivergences found. Finally, to date neonatal matching oftongue protrusion is widely accepted as a phenomenon(Anisfeld, 1996; Meltzoff & Moore, 1997), but stillremains controversial in its interpretation as imitation.

A 2D stimulus design may help investigate alternativeinterpretations. In our study, newborns were presentedwith 2D animated models composed of tongue protru-sions displayed by a human face, a disembodied humanmouth and a disembodied robotic mouth protruding anartificial tongue. Since numerous studies have alreadydemonstrated that newborns are able to match differentfacial gestures (e.g. mouth opening, tongue protrusion,lip protrusion) and discriminate between them, our studydid not use a cross-target method but instead included

Address for correspondence: Robert Soussignan, Centre des Sciences du Go�t et de l’Alimentation, CNRS UMR 6265, 1324 INRA-uB, 15 rue HuguesPicardet, 21000 Dijon, France; e-mail: robert.soussignan@u-bourgogne.fr or Jacqueline Nadel, Centre Emotion, CNRS, USR 3246, PavillonCl�rambault, H�pital de la SalpÞtri�re, 47 Bvd de l’H�pital, 75013 Paris, France; e-mail: jacqueline.nadel@upmc.fr

� 2010 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.

Developmental Science 14:2 (2011), pp 385–394 DOI: 10.1111/j.1467-7687.2010.00984.x

several models of the same movement (tongue protru-sion) so as to achieve a rigorous examination ofparameters that control the matching response. Besidestesting the effect of a 2D action observation on a 3Daction execution, such an experimental addition to theclassical tongue protrusion procedure allows us toexamine more clearly the different theories supporting orrejecting imitation as being a specific capacity alreadypresent at birth, or even the matching phenomenon itself.There are four options: the active intermodal mapping(AIM) model, the associative sequence learning (ASL)model, the innate releasing mechanism (IRM) model andthe exploratory behavior hypothesis.

Theoretical interpretations of neonatal matchingbehavior

AIM model

Challenging Piaget’s (1945) earlier denial of any suchcapacity in newborns, the matching phenomenon wasinterpreted as an early expression of imitation byMeltzoff and Moore (1977, 1983) and by almost allresearchers who replicated the phenomenon (see Nadel &Butterworth, 1999). Meltzoff and Moore (1997) pro-posed that the origin of this capacity is to be found in arepresentational mechanism that codes perceived andproduced movements within a common supra-modalframework which enables newborns to detect and rec-ognize equivalences between the felt but unseen move-ments of the self (proprioceptive feedback) and the seenbut unfelt movement of others (visual input). Thisintermodal capacity, however, is not fully efficient at first.According to AIM theory and data, newborns begin theresponse period by making small tongue movementsinside the mouth and then gradually correct the move-ments until they perform full tongue protrusion (Meltz-off & Moore, 1983, 1997). Such description of aprogressive adjustment of motor execution to visualobservation raises the possibility that the underlyingmechanism of active perception–action coupling mightbe mediated by the activity of the so-called mirror neu-ron system (MNS). Given the plasticity of MNS evi-denced in adults (Calvo-Merino, Glaser, Gr�zes,Passingham & Haggard, 2005), and the similarity ofactivation shown by infants during action-observationand action-execution (Nystrçm, 2008), one could spec-ulate that a proto-MNS might be functional in the firststages of development (Lepage & Th�oret, 2007).

ASL model

An alternative option, based on the ASL model, devel-ops the idea that the capacity to imitate is not a specificmechanism but rather is part of a general process ofassociative learning. According to this model, the mirrorproperties of the MNS are not intrinsic but ratherdepend on experienced contingency between stimulus

and responses (Catmur, Walsh & Heyes, 2007). ASLpostulates that the image guiding action is composed oftwo action representations, one encoding visual informationand the second containing somatic-sensory informationand motor commands, with direct associations betweenboth, due to repeated sensory-motor experiences (Heyes,2001). In the case of neonatal imitation, sensory-motorassociations might take place within a short-term expe-rience of repeated presentations of tongue protrusion.However, the purely associative view leaves many crucialquestions unanswered, especially from a developmentalviewpoint. For instance, on which signal do newbornsrely to associate their motor output with the corre-sponding visual input? When newborns are looking at atongue protrusion how can they know that only one ofthe movements that they have produced earlier matchesthat of the model? In order to create such associations,the spontaneous production of infants’ tongue protru-sion would need to be systematically followed by themodel tongue protrusion: Only in this case could themotor output and the visual stimulation be coupled.Theoretically, it is possible to create any type of associ-ation. Infants can respond to the model’s mouth openingwith a tongue protrusion and vice versa. However, noone has tested this experimentally.

IRM model

Although differing on the origin of neonatal matching,AIM and ASL both see such capacities as relying onrepeated attempts to couple perception and action. Bothmodels differ from what the IRM view would suggest.This model postulates that neonatal matching is drivenby an inborn response restricted to a single oral move-ment (tongue protrusion) elicited by a delimited class ofstimulation (Anisfeld, 1996; Jacobson, 1979). Within thisframework, repeated exposure to tongue protrusionshould not improve matching efficiency. At this point wemust note that studies exploring the IRM view have notyet provided any conclusive results: Jacobson (1979)reported in 6–14-week-olds that a moving pen was aseffective as the tongue model in eliciting tongue protru-sion, but Abravanel and DeYong (1991) using a puppet-mouth with 3–7-week-olds, and Legerstee (1991) using ared object moving back and forth in 5–8-week-olds, didnot replicate the findings.

Exploratory behavior hypothesis

Jones’s view (1996) suggests that infants’ tongueprotrusion is a general exploratory response to any suf-ficiently interesting ⁄ arousing stimuli. Within this per-spective, tongue protruding is a precursor of mouthingand infants do not match tongue protrusion, but theyjust explore the moving stimulus via an oral behavior: thematching is coincidental. Jones (1996, 2006) reportedincreased rates of tongue protrusion in infants exposedto novel non-human visual displays and to music. This

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hypothesis, however, cannot explain why infants not onlymatch ordinary tongue protrusion but also tongue pro-trusion to the side, as shown by Meltzoff and Moore(1994). Jones (2006) also indicated that mouthingmovements habituate with model-specific repetition andrecover with the introduction of a physically differentobject. If so, there should be a decrease of tonguemovements through repeated exposure to tongue pro-trusion. Note that Jones’s studies included infants aged4 weeks and not newborns.

Current study

The present study was aimed at examining the conditionsof tongue protrusion matching by comparing the effectsof three 2D protruding tongue stimuli: a woman’s face, adisembodied woman’s mouth and a robotic mouth pro-truding an artificial tongue. Equalized for contrast,luminance, dimension and color, as well as for thedynamic and spatial features of tongue protrusion(amplitude, duration, velocity, rhythm, and direction),our design appears to us to be an adapted tool to tacklethe following questions:

1. Do newborns match a 2D stimulus of tongue pro-trusion? Note that until now, numerous experimentshave used 2D stimuli to study neonatal visual explo-ration and preferential looking, but none to ourknowledge to assess matching behaviors. A positiveanswer to this question would open the door tonumerous novel experimental designs. Although 2Dstimuli might be less suggestive than 3D ones (Zack,Barr, Gerhardstein, Dickerson & Meltzoff, 2009), ourhypothesis is that they should nevertheless enhancematching behavior.

2. What would be the predictions for the four optionssupporting or rejecting the imitation hypothesis? Aparameter that differentiates the four options con-cerns the rate of newborns’ tongue protrusion overtime. The ASL model predicts an increase of tongueprotrusion over time, as the sensorimotor associationsare reinforced by repeated exercise and the contingentassociations, if any, are the same for the three pro-truding stimuli. More discriminative, the AIM modelpredicts an increase of tongue protrusion rate andmore progressively accurate matching after repeatedspecific exercise of each specific stimulus, due tointermodal mapping. By contrast, the IRM modelpredicts no change of rate over time since thematching behavior is seen to be stimulus-triggered.Finally Jones’s hypothesis predicts a decrease oftongue protrusion rates, due to a decrease of interestby repeated presentation of the same movement, andan increase of tongue protrusion when the stimuluschanges engendering an increase in interest.

Whether or not newborns match tongue protrusion ofdisembodied mouths also discriminates some of the fourpositions. AIM, ASL and IRM models are compatible

with a positive answer to this question. By contrast,Jones’s position should favor the tongue protruding froma full human face as the most complex ⁄ interestingstimulus to generate tongue protrusion, since infantsprefer top-heavy patterns (Cassia, Turati & Simion,2004) and complex visual patterns (Miranda & Fantz,1971).

As for the possibility that newborns match theartificial tongue protruded by a robotic mouth, all fouroptions are compatible with a positive answer, fordifferent reasons. IRM will stress the releasing aspect ofmatching. The exploratory behavior hypothesis putsforward the interest in exploring this moving object.AIM and ASL will argue that recent studies haveevidenced similar MNS responses to robotic and bio-logical movements when the mechanical motion is closelymatched with the biological one (Bird, Leighton, Press &Heyes, 2007; Gazzola, Rizzolatti, Wicker & Keysers,2007; Press, Bird, Flach & Heyes, 2005; Oberman,McCleery, Ramachandran & Pineda, 2007). Though notdiscriminating the four positions, the possible matchingof a robotic tongue protrusion is interesting per se: so farwe do not know how newborns respond to the 2Dperception of protruding movements done by amechanical device. Presenting a disembodied artificialtongue could help provide some initial explorations ofthis question. Note that the temporal dynamics of themovement of the artificial tongue protrusion weredesigned to closely match the human mouth tongueprotrusion. The background was also closely matched byhaving the artificial tongue protrude from the sameflesh-toned background as the human one.

Method

Participants

Forty-five newborns (18 boys, 27 girls) less than 90 hoursold (range: 1.82–87 hours) participated in the experimentat the maternity unit of the Ambroise Par� Hospital,with the written informed consent of the parents. Theyall fulfilled the following inclusion criteria: normaldelivery, no detected infection, no visual or motorabnormalities, gestational age greater than 36 weeks,Apgar score of at least 8 at 5 min, and birth weight morethan 2500 g. They had been fed within the previous2 hours and displayed a behaviorally calm state for 5 minimmediately prior to testing. From this sample, 12infants were excluded due to fussiness, sleepiness orhiccupping during the experiment. Fifteen infants wereexcluded after coding because they were unable toestablish a visual attention of at least 6 s toward thestimulus for each of the four conditions. This rate ofattrition has often been reported in previous studies withnewborns (e.g. Kessen, Salapatek & Haith, 1972;Meltzoff & Moore, 1989). The 18 newborns (13 girls, fiveboys) retained for the study had an average age of

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38.14 hours (SD = 21.5) at the time of testing and amean birth weight of 3640 g (SD = 304). The meangestational age at birth was 39.5 weeks (SD = 0.97), andthe mean 5-min Apgar score was 9.89 (SD = 0.47). Theexperiment was conducted on average 47.2 min(SD = 48.1) after the last feed to avoid tongue protru-sion due to a preprandial state (Soussignan, Schaal &Marlier, 1999).

Setting and apparatus

Testing took place in a quiet and unoccupied bedroom ofthe maternity hospital with a dim level of light. Thenewborns were seated in a 25� reclining infant chair thatsupported their trunk and shoulders and positioned thehead slightly at the back so as to allow head or eyemovements toward the screen without great effort. Thehead was at a distance of 30 cm from a 19-inch flatscreen fixed on the front of the bed by an articulated arm(Ergotron LX) enabling the alignment of the newborn’seye level to the center of the screen. In front of thenewborn’s face but out of her ⁄ his visual field, a videocamera (Sony DCR-HCR96E) mounted below thescreen provided accurate recordings of the infant’sface. A 15-inch laptop computer connected to thescreen allowed an experimenter to control the stimulusonset.

Stimuli and experimental design

Four digitalized video clips were used (see Figure 1). Onewas the picture of a static blue cube presented during thebaseline period. This stimulus was selected (i) for visualcalibration in allowing newborns to focus on the sameobject shape before presenting them with the threedynamic stimuli and (ii) to have a control static condition

as in previous in vivo studies. The dynamic video clipswere models of tongue protrusion (TP) displayed by (a) ahuman face (HF), (b) a human tongue (HT) from adisembodied mouth and (c) an artificial tongue (AT)from a robotic mouth. All recordings were equalized inlighting conditions (1000 W spotlight). The four stimuliwere inserted on the same background which was thecolor of human skin.

The robotic mouth protruding an artificial tongue wasan improved version of a mechanical device previouslybuilt in collaboration with roboticists (Potier, Viezzi,Gaussier & Nadel, 2002). The HT and the AT as well asthe cube were positioned at the center of the screen. At aviewing distance of 30 cm, the cube subtended a visualangle of 9.55 · 9.55�, and the three mouths displayingTP subtended a 9.55 · 7.64� visual angle. The viewingangle for the face was 47.75 · 34.38�.

The four clips were assessed for contrast differencebetween the background and the target object. AdobePhotoshop CS2 software was used to extract five levels ofcontrast for each stimulus: +50%, +25%, 0%, )25%, and)50%. The contrast difference between the backgroundand the target object in the 20 pictures was rated by 10adults (age: M = 29 years, SD = 6.48) on a 9-pointLikert scale [from 1 (extremely weak) to 9 (extremelyhigh)]. A two-way analysis of variance (ANOVA) withstimuli (four) and levels of contrast (five) as the within-subjects variables indicated, as expected, that the judgesperceived significant differences between the five levels ofcontrast, F(4, 36) = 156.9, p < .0001. However, no effectof interaction between the target objects and the levels ofcontrast was detected (p > .05), indicating that the fourtarget objects selected in our experiment were judged asequivalent in their degree of contrast (cube: M = 5.0,SD = .67; HF: M = 5.7, SD = .82; HT: M = 5.2,SD = .79; AT: M = 5.5, SD = .53).

(a) (b) (c) (d)

Figure 1 Sample photographs from videotape recordings: (a) baseline condition (cube) and tongue protrusions demonstrated bythree models: (b) human mouth, (c) robotic mouth with artificial tongue, and (d) full human face.

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The temporal structure of the TP demonstration per-iod was matched for the three protruding conditionsusing the Adobe Premiere Pro software. The TP waspresented at a rate of three times per 6-second interval.Each TP demonstration period corresponding to a burstwas repeated four times (named burst 1, burst 2, burst 3,and burst 4) and alternated with a still period of 3 or6 seconds. The total duration of each dynamic displayand of the baseline condition was 42 seconds. Theschematic diagram of the TP bursts and of the stillperiods is illustrated in Figure 2. The four video clips ofbaseline condition (BC) and dynamic displays were thenassembled and the onset and offset of each 42-secondcondition were signaled by including in the audio chan-nel of the video clip a 40-ms tone of 1500 Hz (onset) and2000 Hz (offset). Six combinations of the three stimuliwere created to yield six presentation orders counter-balanced across the participants: HF-HT-AT, HF-AT-HT, HT-HF-AT, HT-AT- HF, AT-HT-HF, and AT-HF-HT.

Procedure

The infant was placed by the mother in the seat in frontof the screen while the newborn was in a quiet, alert state.The mother stood behind the infant’s seat and was askedto refrain from any talk and physical contact with herinfant during the experiment. The experimenter adjustedthe newborn’s eye level to the center of the screen. At thebeginning, the static color cube (baseline condition) wasdisplayed. As soon as the experimenter had verified thatthe infant fixated the screen around the stimulus (i.e. theexperimenter monitored whether the infant’s gaze wasdirected toward the center of a 2.7 LCD screen of thecamcorder), he initiated a trial by pressing a key on thecomputer. The onset of the experiment was signaled tothe experimenter by a sound through an earphone thatwas connected to the video-camera microphone. Thethree dynamic stimuli were displayed in a counterbal-anced order across the participants. The static cube (BC)was always presented at the beginning of the experimentand was not included in the counterbalanced design inorder to have a true baseline condition and avoid anyresponse that could be a delayed reaction to a previouslypresented dynamic stimulus (Meltzoff & Moore, 1989).

Coding and statistical analysis

The video recordings of infants’ behavior were digital-ized and coded using a revised version of the Elansoftware (Bickford, 2005; Grynszpan, 2006). This soft-

ware allows an analysis of behavioral items on separatechannels of the Elan window and a recording of time(latency, duration) and occurrence of behavioral events.The coding of video records was performed in two steps.During the first step, a coder, blind to the type of stim-ulus viewed by the newborn and unaware of the pre-sentation order, scored in real time and frame-by-framethe TP and mouth opening (MO) of the infants as well asgaze toward the screen. Both partial and full TP werecoded. A full TP was scored when the tongue tip clearlycrossed the back edge of the lower lip. A partial TP wasoperationally defined as a forward movement of thetongue such that the tongue tip was between the lips ormoved forward in the open mouth but not beyond thelips. Mouth opening was scored when a visible downwardmovement of the lower jaw parted the newborn’s lips.The infant’s gaze toward the screen was used as an indexof visual attention and was defined as the time duringwhich the newborn directed her ⁄ his open eyes toward thescreen. It included eye movements and fixations. Eyemovements were defined as saccades relocating eye fix-ations and scored in number of saccades. Excluded fromthe analysis was any time in the experiment that occurredduring yawning or sneezing.

In sum, the dependent variables derived from thesemeasures were the frequency of TP expressed in rate perminute (number of occurrences of TP ⁄ duration ofobservation during which the infant was in an alert state* 60), the frequency of MO expressed in rate per minute(number of occurrences of MO ⁄ duration of observationduring which the infant was in an alert state * 60), thepercent of time the infants looked at the screen (durationof infant’s gazing at the screen ⁄ duration of observationduring which the infant was in an alert state), and thefrequency of eye movements in rate per minute (numberof saccades ⁄ duration of gazing at the screen * 60).

During the second step, the temporal occurrences ofinfant’s TP and MO were compared to the onset time ofTP displays. The frequency of these facial gestures fol-lowing each burst plus the still phase of each burst (burst1, burst 2, burst 3, and burst 4) was then computed foreach dynamic display (number of occurrences ⁄ durationof burst period * 60).

Inter-observer reliabilities were assessed with a secondcoder who scored a randomly selected 30% of the data.The second coder was also blind to the order and natureof stimuli shown to the infant in any given period ofdemonstration. For TP and MO, Cohen’s kappa coeffi-cients of inter-observer reliability were calculated byscoring for the two coders an infant’s response thatoccurred within the same second. Kappa values were .76for the occurrences of partial and full TP and .78 for theoccurrence of MO. The Pearson correlations were .97for the duration of visual attention and .90 for the fre-quency of eye movements toward the stimuli. Repeated-measures ANOVAs were performed on measures of TP,MO, visual attention and eye movements. Tukey’s HSDtests were used for post-hoc multiple comparisons

Figure 2 Schematic diagram of the demonstration periods(bursts) of tongue protrusions for each dynamic display.

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between means. Partial eta-squared (g2p) and Cohen’s d

were reported as a measure of effect size in ANOVAs andin the comparisons between the means, respectively,where d = M1)M2 ⁄ spooled, and spooled = �[(s1

2 + s22) ⁄ 2]

(Cohen, 1988). Cohen (1988) suggested the meanings ofdifferent effect sizes, with small effect sizes as d = .2,medium as d = .50, and large as d = .80.

Results

Comparison of TP frequencies according to the type ofstimulus

The frequencies of TP were submitted to a two-wayANOVA, with the type of stimulus (BC, AT, HT, andHF) and the type of TP (partial vs. full infant response)as the within-subjects variables. A significant maineffect for the type of stimulus was found, F(3,51) = 4.81, p = .005, g2

p = .22. Tukey’s HSD compar-ison tests revealed that infants produced more TP whenthe dynamic display was the HT (p = .003, d = .87) orthe AT (p = .03, d = .78) as compared to the BC (seeFigure 3). However, contrary to our expectation, HFdid not induce a significant increase of TP as comparedto the BC (p = .09). The interaction between the type ofstimulus and the type of TP failed to reach significance(p > .05).

Frequencies of TP according to the rank of protrusionburst

The frequencies of TP produced by the newborns inresponse to each burst of dynamic display were submit-ted to a three-way ANOVA with the type of stimulus (AT,HT, HF), the type of TP (partial, full) and burst rank(B1: burst 1, B2: burst 2, B3: burst 3, and B4: burst 4) asthe within-subjects variables. No significant main effectsemerged (all ps > .05). However, the interaction betweenthe type of TP and the burst rank was significant, F(3,51) = 3.93, p = .01, g2

p = .19, indicating that infantsdisplayed a higher rate of full TP following the presen-tation of the fourth than the first (Tukey’s HSD test,p = .03, d = .75) or the second (Tukey’s HSD test,p = .02, d = .85) burst of TP (see Figure 4). In contrast,the rates of partial TP did not change significantly as thefunction of the burst rank. The interaction between theother factors failed to reach significance (p > .05).

To further demonstrate that our findings reflectedmatching responses to modeled gesture conditions andnot a non-specific arousal response to moving stimuli,the effect of the presentation order of dynamic displays(task order) on TP frequencies was tested. The dynamicstimuli presented first was defined as the first task (T1),those presented second as the second task (T2) andthose presented last as the third task (T3). A two-wayANOVA performed on infants’ TP, with type of TP(partial, full) and presentation order of stimuli (T1, T2,T3) as within-subjects variables did not indicate signif-

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5

6

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Figure 3 Mean frequencies (with standard errors bars) ofnewborns’ tongue protrusion (TP) during the four conditions(BC: baseline condition, AT: artificial tongue from a roboticmouth, HT: human tongue from a mouth, HF: tongue from ahuman face). *Significant at p < .05; **significant at p < .005.

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Figure 4 Mean frequencies (with standard errors bars) ofnewborns’ partial (……) and full (_____) tongue protrusion (TP)as a function of the burst rank of the TP displayed by theprotruding models (B1: Burst 1, B2: Burst 2, B3: Burst 3, B4:Burst 4). *Significant at p < .05.

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icant main effects for the presentation order [F(2,34) = .96, p = .38; T1: M = 5.63, SD = 3.74; T2:M = 6.98, SD = 7.01; T3: M = 5.23, SD = 4.82], andfor the type of TP, F(1, 34) = .09, p = .76. The inter-action between these variables also failed to reach sig-nificance, F(2, 34) = 2.48, p = .1. Thus, it can beconcluded that the newborns did not increase their TPas the function of the exposure to the cumulated effectof moving displays throughout the three tasks, but thatthe rate of infants’ responding was affected by therepeated presentation of each modeled protrudingcondition.

Frequencies of mouth opening

To examine whether TP was indeed a selective facialresponse that was matched to the modeled act, anANOVA was conducted on the frequencies of newborns’MO with the type of stimulus as the within-subjectsvariable. No significant main effect of the type ofstimulus was found for this facial gesture, F(3, 51) = .16,p = .92 (BC: M = 1.36, SD = 1.15; HF: M = 1.41,SD = 2.02; HT: M = 1.32, SD = 1.74; AT: M = 1.12,SD = 1.05). The frequencies of newborns’ MO inresponse to each burst of dynamic display were alsosubmitted to a two-way ANOVA with the type of displayand burst rank as the within-subjects variables. Theeffects for dynamic display, F(2, 34) = .18, p = .83, andburst rank, F(3, 51) = .64, p = .59 (B1: M = .90,SD = 1.59, B2: M = 1.62, SD = 2.35, B3: M = 1.36,SD = 1.72, B4: M = 1.49, SD = 1.79) were not signifi-cant, nor was the interaction between these variables,F(6, 102) = .94, p = .47. Finally, the effect of the pre-sentation order of dynamic displays (T1, T2, and T3) wastested on infants’ MO frequencies. The ANOVA failed toindicate that MO increased with the cumulated effect ofmoving displays throughout the three tasks, F(2,34) = .28, p = .76 (T1: M = 1.23, SD = 1.64; T2:M = 1.48, SD = 1.83; T3: M = 1.13, SD = 1.47).

Attention to visual stimuli

An ANOVA was performed on the percentage of lookingtimes to the screen, with the type of stimulus as thewithin-subjects variable. Although on average newborninfants spent more time looking at the HF (M = 87%,SD = 12.82) than at the other stimuli (BC: M = 79.78%,SD = 19.79; AT: M = 81.61%, SD = 15.25; HT:M = 78.53%, SD = 18.18), no significant difference wasdetected, F(3, 51) = .99, p = .40. However, an ANOVAconducted on the frequency of infants’ eye movementsrevealed a main effect of the type of stimulus, F(3,51) = 2.86, p = .04, g2

p = .14. Pairwise comparisonsusing Tukey’s HSD tests indicated that newbornsexhibited more eye movements to the HF (M = 23.47,SD = 7.53) than to the BC (M = 16.71, SD = 6.31),p = .02, d = .97, whereas no significant difference wasdetected between the other dynamic displays and the

baseline condition (AT: M = 18.60, SD = 9.40; HT:M = 19.21, SD = 7.83).

Finally, the percentage of time the infants spent gazingat the screen did not change as a function of the length ofexperiment, when using the presentation order of thetask as the within-subjects variables in an ANOVA, F(3,51) = .66, p = .58. The baseline condition was used asthe first task (T1), the dynamic stimuli presented secondas the second task (T2), and so on for those presentedthird (T3) and fourth (T4). Hence, it can be concludedthat the infants were similarly attentive to each conditionand that their attention did not decrease throughout theexperiment.

Discussion

We used an innovative experimental design that revealedthe capacity of 1- to 3-day-old infants to match tongueprotrusion produced by 2D stimuli. Disembodiedmouths displaying biological movements of a tongue orwell-matched movements from an artificial tongue werefound to elicit matching responses. Results also indicatedthat matching improved through repetition of the stim-ulus. This was documented by the increase of full tongueprotrusions together with a stable rate of partial pro-trusions. Moreover, the improvement was found for eachkind of stimulus, thus accounting for a discriminativeintermodal mapping. These findings have implicationsfor theoretical frameworks and possible mechanisms ofneonatal matching phenomena.

Overall, our study shows that newborns increase theirtongue protrusion when seeing televised tongue protru-sions, as they would do when seeing a person protrudinghis ⁄ her tongue. Furthermore, they produced equivalentmean rates of tongue protrusion per minute (AT = 5.65;HT = 6.74; HF = 5.16) compared to those reported inprevious studies using the live procedure in 1- to 3-day-old human infants (Heimann, 1989: 4.91; Meltzoff &Moore, 1989: 6.73; Vinter, 1986: 4.13). Thus, despiteinfants showing a preference for 3D over 2D stimuli (e.g.Slater, Rose & Morison, 1984), the two-dimensionalperception of protruding stimuli also generates matchingbehavior in newborn infants. This is an interesting resultper se, that may encourage further exploration of theneonatal capacity to match ⁄ imitate a range of move-ments (lip protrusion, mouth opening, eye blinking,finger movements, and emotional expressions) in well-controlled conditions.

Matching response to disembodied human and roboticmouths

The overall pattern of data provides the first evidencethat a mouth disembodied from a face configuration anddisplaying tongue protrusion is an effective stimulusfor eliciting similar movements in newborns. This sug-gests that the whole perceptual information embedded

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within a face is not necessary for eliciting neonatalmatching behavior and that a relationship with a humanpartner is not a required condition. The finding that ahuman tongue protrusion disembodied from the per-ceptual context of a face produced matching responses,as stressed by the AIM model, suggests that perceptionof localized movements might be considered a criticalfeature for activating the observation–execution match-ing system (Meltzoff & Moore, 1997). By contrast andunexpectedly, the perception of a full 2D face protrud-ing a tongue did not induce a significant increase ofinfants’ tongue protrusion as compared with the base-line condition although the trend was in the correctdirection. This cannot be explained by a reduction ofvisual attention toward the human face since no sig-nificant difference was found for infants’ gaze amongthe four conditions. A conflict between different facialregions of interest might be in play. It is now establishedthat neonates are able to discriminate the inner featuresof a face (Simion, Farroni, Cassia, Turati & Barba,2002; Turati & Simion, 2002), and prefer photographsof real faces with eyes open rather than closed (Batki,Baron-Cohen, Wheelwright, Connellan & Ahluwalia,2000), or faces with direct rather than averted gaze(Farroni, Csibra, Simon & Johnson, 2002). Newborninfants should thus attribute more interest to a face thanto an isolated mouth. On the other hand, the role ofmovement in visual attention at birth is well docu-mented (Slater, Morison, Town & Rose, 1985) andconstitutes a fundamental property for eliciting match-ing behavior (Vinter, 1986). Thus, it is possible thatwhen confronted with two highly attractive inner com-ponents of the human face (eyes and tongue move-ment), newborns might have explored different featuresof the face instead of focusing on tongue movementthus distracting their attention from the tongue. Thishypothesis is supported by the fact that infants in ourstudy showed more eye movements toward the full facedisplay suggesting that they spent more time exploringthe inner facial features.

Our results also reveal that an artificial tongue is anefficient stimulus with which to elicit tongue protrusionmatching. The finding that a robotic mouth protrudingan artificial tongue which emerges from a skin-coloredbackground is sufficient to induce matching responsessupports the hypothesis that the detection of similarpatterned movement directed towards self as well as therhythmical properties of object movement might bepowerful elicitors of tongue protrusion (Zazzo, 1957).Although we cannot be sure whether such responseswould be similarly elicited by other movement patterns,this result is in line with neuroscience research thatinvestigates the neural basis of action–perception cou-pling in adults facing robotic actions. Recent studiesusing high temporal (EEG) and spatial (fMRI) resolu-tion techniques highlighted that the sight and imitationof both human and robotic actions resulted in suppres-sion of the mu rhythm of the sensorimotor cortex

(Oberman et al., 2007) or strongly activated corticalstructures of the MNS (Gazzola et al., 2007).

Our 2D design offered a relevant test of the IRMmodel via the use of equalized biological and mechanicalstimuli. Although the neonatal matching of the artificialtongue might be compatible with the IRM model, ourfinding of a clear effect of the repetition of each stimuluson matching response is at variance with the core pre-diction of this view, namely that certain stimulus con-figurations innately and automatically trigger fixedpatterns of behavior without any learning (Anisfeld,1991).

Accurate matching response to repetitive exposures ofmodeling periods

Our results provide strong evidence that 1- to 3-day-oldnewborns progressively increased tongue protrusion inresponse to repetitive exposures to each modeled act. Foreach stimulus condition, newborns increased signifi-cantly the rate of matching responses following the pre-sentation of the fourth burst as compared with the firstand the second bursts of tongue protrusion. More spe-cifically, they displayed an increase of full tongue pro-trusion, and not of partial ones or of mouth opening,following the fourth burst. This suggests that they pro-vided more accurate matching and probably correctedtheir facial gesture as a consequence of the repeatedexposure within each stimulus presentation (Meltzoff &Moore, 1997). A similar finding was reported for new-borns’ index finger movements that showed gradualrefinement toward the modeled act following successivedemonstrations (Nagy et al., 2005). Such findings cannotbe merely explained by a non-specific arousal response tomoving displays or by exploratory behavior. A non-specific arousal hypothesis would predict an increase oftongue movements as the consequence of the duration oftime in the experiment or of the cumulative exposure to amoving display. By contrast, our data showed no evi-dence of a carry-over effect from one dynamic conditionto the next since the order of task presentation did notaffect the frequency of tongue protrusion. This suggeststhat infants became more accurate as a function of thesuccessive presentation of a given stimulus and had tolearn again for another stimulus. Similarly, the overallpattern of our findings does not fit Jones’s exploratoryhypothesis (1996, 2006) since, contrary to this hypothesis,the more visually explored stimulus (human face) did notinduce the highest rate of tongue movements, and thelast burst of dynamic displays did not elicit a decrease oftongue protrusion rates.

Our findings suggest that the action observation–execution matching mechanism is not stimulus-boundor reflex-like at birth, as proposed by the IRM model,but rather is experience-dependent and relatively flexi-ble, as the AIM and ASL models would predict (Heyes,2001; Meltzoff & Moore, 1997). Although the AIM andASL models differ regarding the mechanisms under-

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lying facial matching ⁄ imitation (AIM: a dedicatedsupramodal representational system; ASL: a generalprocess of Hebbian learning), they are both concordantwith the view that infants’ matching responses mayincrease over successive trials (Meltzoff & Moore, 1994,1997), or that the simultaneous activation of observedand executed acts can create associations that willbecome stronger with repetitive exposures over time(Brass & Heyes, 2005; Heyes, 2001). However, as theAIM model predicted, infants did not immediatelydisplay accurate matching to the first presentations ofthe modeled behavior, but instead they needed tocorrect their tongue protrusion to achieve it (Meltzoff &Moore, 1994). Ultimately, our data fully correspond towhat the AIM model would predict about progressiveachievement of the matching behavior (Meltzoff &Moore, 1994). It has been proposed that the percep-tion–action coupling mechanism present at birth ismediated by a rudimentary MNS (Lepage & Th�oret,2007). Studies are needed using neuroscience techniquesto empirically test this hypothesis in human newbornsexposed to 2D or 3D modeling conditions.

Acknowledgements

This research was funded by the European Union ProjectFeelix Growing IST. We are deeply grateful to the staff ofthe Ambroise Par� Maternity hospital for their efficientcollaboration with the experiment and the parents andnewborns for their kind participation.

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Received: 17 October 2009Accepted: 15 April 2010

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