# Do Parentese Prosody and Fathers' Involvement in Interacting Facilitate Social Interaction in Infants Who Later Develop Autism?

David Cohen, Raquel S Cassel, Catherine Saint-Georges, Ammar Mahdhaoui, Marie-Christine Laznik, Fabio Apicella, Pietro Muratori, Sandra Maestro, Filippo Muratori, Mohamed Chetouani

<figure><img src="image_1.png" /></figure>

## To cite this version:

David Cohen, Raquel S Cassel, Catherine Saint-Georges, Ammar Mahdhaoui, Marie-Christine Laznik, et al.. Do Parentese Prosody and Fathers' Involvement in Interacting Facilitate Social Interaction in Infants Who Later Develop Autism?. PLoS ONE, 2013, 8 (5), pp.e61402. 10.1371/journal.pone.0061402. [hal-01618730](https://hal.sorbonne-universite.fr/hal-01618730v1)

HAL Id: hal-01618730

https://hal.sorbonne-universite.fr/hal-01618730v1

Submitted on 18 Oct 2017

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_2.png" /></figure>

Distributed under a Creative Commons CC BY 4.0 - Attribution - International License
# Do Parentese Prosody and Fathers' Involvement in Interacting Facilitate Social Interaction in Infants Who Later Develop Autism?

David Cohen¹,²*, Raquel S. Cassel¹,², Catherine Saint-Georges¹,², Ammar Mahdhaoui², Marie-Christine Laznik³, Fabio Apicella⁴, Pietro Muratori⁴, Sandra Maestro⁴, Filippo Muratori⁴, Mohamed Chetouani²

1 Department of Child and Adolescent Psychiatry, Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière, Université Pierre et Marie Curie, Paris, France, 2 Institut des Systèmes Intelligents et de Robotique, Centre National de la Recherche Scientifique UMR 7222, Université Pierre et Marie Curie, Paris, France, 3 Department of Child and Adolescent Psychiatry, Association Santé Mentale du 13ème, Paris, France, 4 Division of Child Neurology and Psychiatry, University of Pisa, Stella Maris Scientific Institute, Calambrone, Italy

## Abstract

**Background:** Whether development of autism impacts the interactive process between an infant and his/her parents remains an unexplored issue.

**Methodology and Principal Findings:** Using computational analysis taking into account synchronic behaviors and emotional prosody (parentese), we assessed the course of infants' responses to parents' type of speech in home movies from typically developing (TD) infants and infants who will subsequently develop autism aged less than 18 months. Our findings indicate: that parentese was significantly associated with infant responses to parental vocalizations involving orientation towards other people and with infant receptive behaviours; that parents of infants developing autism displayed more intense solicitations that were rich in parentese; that fathers of infants developing autism spoke to their infants more than fathers of TD infants; and that fathers' vocalizations were significantly associated with intersubjective responses and active behaviours in infants who subsequently developed autism.

**Conclusion:** The parents of infants who will later develop autism change their interactive pattern of behaviour by both increasing parentese and father's involvement in interacting with infants; both are significantly associated with infant's social responses. We stress the possible therapeutic implications of these findings and its implication for Dean Falk's theory regarding pre-linguistic evolution in early hominins.

**Citation:** Cohen D, Cassel RS, Saint-Georges C, Mahdhaoui A, Laznik M-C, et al. (2013) Do Parentese Prosody and Fathers' Involvement in Interacting Facilitate Social Interaction in Infants Who Later Develop Autism? PLoS ONE 8(5): e61402. doi:10.1371/journal.pone.0061402

**Editor:** Stephanie Ann White, UCLA, United States of America

**Received** November 5, 2012; **Accepted** March 8, 2013; **Published** May 1, 2013

**Copyright:** © 2013 Cohen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

**Funding:** The Pisa "home video in autism" project was supported by grants PRIN 2003-2005 and PRIN 2005-2007 from the Italian Ministry of Instruction, University, and Research. The current study was supported by a grant (n° 2008005170) from the Fondation de France given to MC and DC, by the Université Pierre et Marie Curie (Projet Emergence 2010) the European Commission (FP7: Michelangelo under grant agreement n° 288241), and the fund "Entreprendre pour aider". The funding agencies and the University were not involved in the study design, collection, analysis and interpretation of data, writing of the paper, or the decision to submit for publication.

**Competing Interests:** The authors have declared that no competing interests exist.

* E-mail: david.cohen@psl.aphp.fr

## Introduction

Autism spectrum disorders (ASD) are developmental disorders that are characterised by the presence of symptoms in 3 domains: (i) abnormalities in reciprocal social interactions; (ii) abnormalities in patterns of communication; and (iii) a repetitive repertoire of behaviours and interests. ASD are heterogeneous in terms of clinical manifestations and course, but children's difficulties with adequate socialization or communication are at the core of the pathologic developmental course. The most typical form of ASD is autism that presents with symptoms in all 3 domains and has an early age of onset (before 3 years). Symptoms, such as speech delay and stereotyped behaviour, are often evident between 18 and 36 months, but these clearly are not the initial manifestations of autism [1]. Studies using early home videos [2,3] parental

interviews [4] and prospective assessment of siblings of children with ASD [5,6] have revealed atypical developmental tendencies in infants who were later diagnosed with ASD. The first signs are abnormalities with eye contact, imitation, disengagement, joint attention, orienting to name, and body language. These behaviours constitute important precursors of later-developing symptoms; however, whether these first signs impact the interactive process between an infant and their parents and whether they influence the development of the infant himself remain two complex and unexplored issues.

Human learning and cultural evolution are supported by paradoxical biological adaptation. We are born immature; yet, immaturity has value: "*Delaying maturation of cerebral cortex allows initial learning to influence the neural architecture in ways that support later,*
more complex learning” [7]. Early learning appears to be computa-
tional [8] and to be based on perceptual-action mapping [7].
Learning is also social [9] and supported by skills present in
infancy: imitation, shared attention and empathic understanding
[7]. The whole social system which contributes to interactional
synchrony and attunement may be disrupted (as explained above)
in infant who will subsequently develop autism.

It is likely that an atypical social trajectory in the infant would affect parents' interactive patterns. However, very few studies have addressed the importance of infant-caregiver synchrony/reciprocity in early interactions involving infants who will subsequently develop autism. Temporally, the interactive nature of human communication implies that a message aᵢ produced by A impacts B who, in return, produces message bᵢ and so on, indicating that some form of reciprocity occurs between partners A and B [10]. Synchrony is difficult to define and delimit. Numerous terms have been used to describe the interdependence of dyadic partners' behaviours (mimicry, social resonance, coordination, synchrony, attunement, chameleon effect, etc.). Here, we define synchrony as the dynamic and reciprocal adaptation of the temporal structure of behaviours between interactive partners [11]. In typically developing children, the quality of social interaction depends on an active dialogue between the parent and the infant based on the infant's desire to be social and the parent's capacity to be attuned [12,13]. Numerous studies have been emphasising the importance of synchrony and the co-modality [14]. In a previous study based on home movies (HM), we showed that when studying interactive patterns with computational methods to take into account synchrony between partners, (i) deviant autistic behaviours appeared before 12 months; (ii) parents seemed to feel weaker interactive responsiveness and mainly weaker initiative from their infants; and (iii) parents increasingly tried to supply soliciting behaviours and touching [15]. It is likely that these modifications of interactive patterns implicate numerous co-influences due to the reciprocal nature of these processes.

A special type of speech directed towards infants, called
'parentese', is characterised by higher pitch, slower tempo, and
exaggerated intonation contours [16]; it appears to be universal
and to play an important role in social interaction and language
development. Parentese has been shown to be present in mothers,
but also in fathers and other caregivers when addressing an infant
[17]. This particular prosody may be responsible for attracting an
infant's attention, conveying emotional affect and providing
language-specific phonological information [16]. Parentese was
found to depend on the quality of the infant's responsiveness,
suggesting that infants are actively involved in the course of
parentese [18,19]. Also, voice-sensitive brain regions are already
specialized and modulated by emotional prosody by the age of 7
months. This raise the possibility that the critical neurodevelop-
mental processes underlying impaired voice processing in autism
might occur early during infancy [20]. Finally, parentese may not
only be crucial during early development but also for species
evolution. Falk proposed parentese to be a key adaptive human
skill during the transition between late australopithecines and early
Homo. This hypothesis is based on the premise that hominin
mothers who vigilantly attended to infants were strongly selected
for and that such mothers had the ability to modify their
vocalisations to control infants who were too immature at birth to
grasp their mothers as chimps do (see the Discussion section for
further exploration of this topic) [19].

Therefore, the study of parentese in early interactions with
infants who will later be diagnosed with autism may provide cues
for understanding the disruption of social and communicative skills
in children with autism. We postulated that if learning and

development depend on normal social interest in people and the
signals they produce, children with autism, who lack social interest,
may be at a cumulative disadvantage in development and
language learning. Their poor response to parental solicitation
may impair both parental solicitation and parentese production
over time. As a consequence, this impairment will reinforce social
withdrawal and language acquisition delay [21,22].

In this study, we used a computerised algorithm created for the
detection of parentese based on acoustic components [21] and
focused on parents' type of affective speech and infants' responses
simultaneously using HM from two groups: typically developing
(TD) children and children who subsequently developed autism
(AD). We tested the following hypotheses: (H1) as parentese
amplification is bidirectional and children with AD lack social
interest, parentese towards children with AD should decrease over
time; this decrease will likely be greater than that observed in
parentese towards TD children; and (H2) AD infants should be
capable of interacting and responding to parentese at the start of
life. This hypothesis was based on findings from HM studies and
parental interviews showing that the very early behaviours of
infants who later develop autism do not differ dramatically from
typical developing controls [1-5]. A previous exploratory case
study, comparing a TD child and an AD child, supported this
hypothesis: the course of an infant's response to CG vocalization
differed according to the type of speech (motherese vs. other
speech) and child status (TD vs. AD). Mothers spent more time
interacting with infants, and fathers appeared to interact with their
child preferentially between 12 and 18 months in the TD boy [22].
This prompted us to distinguish between mothers' and fathers'
interactive patterns, as such patterns may dramatically differ in
terms of parentese use and time course.

**Materials and Methods**

Overview

The flow diagram of the study is summarised in Figure 1. Thirty
children were randomly selected from the Pisa HM database with
the following criteria: 15 will be diagnosed with AD, and 15 will
develop normally (step 1). All scenes showing a situation in which
social interaction could occur (i.e., all scenes with an infant and an
adult) were extracted and, if necessary, segmented into short
sequences to be scored (step 2). Raters blind to diagnosis rated
parents and infant behaviours independently within each interac-
tion sequence according to a grid with a specific part for each
partner (step 3). To distinguish parents' style of affective speech
according to their emotional and prosodic characteristics, we
classified all parents vocalisations as parentese or other speech (i.e.,
non-parentese) using an automatic algorithm [21]. At this stage,
we lost one child per group because of poor HM audio quality.
Additionally, to distinguish mother vs. father vs. other CG
contributions to CG to infant interactions, we annotated CG
accordingly (step 4). To study specifically how infants responded to
parents' stimulations, we selected any child behaviors occurring
within the 3 seconds following any parents' behavior (step 5). A
generalised linear mixed model (GLMM) was performed to assess
and compare infants' response to parents' vocalisations during
interactive patterns by time and by group (step 6).

Participants (Step 1)

We studied home movies (HM) from the first 18 months of life
of two groups of children that were match for age and sex. The
first group was composed of 15 children (M/F: 10/5) with a
diagnosis of Autistic Disorder (AD) according to the DSM-IV
criteria. In addition, we used the Autism Diagnostic Interview-
<figure><img src="image_3.png" /><figcaption>**Figure 1.** Diagram flow of the study. TD = Typical Development; AD = Autism Disorder; SES = Socio Economic Status; IQ = Intellectual quotient; CARS = Children Autism Rating Scale; CBCL = Child Behavior Check List; SD = Standard Deviation; CG = Care Giver; GLMM = Generalised Linear Mixed Model; \*IQ in children with AD was based on the Griffiths Mental Developmental Scale or the Wechsler Intelligence Scale.
doi:10.1371/journal.pone.0061402.g001</figcaption></figure>

Revised (ADI-R) for diagnosis [23] and the Childhood Autism Rating Scale (CARS) to assess the severity of autistic symptoms [24]. All cases with a CARS total-scores below 30 and with Pervasive Developmental Disorders Not Otherwise Specified were excluded. The absence of an identified genetic or metabolic disorder and of a severe sensory or motor impairment were verified for all children. The AD group was composed of children with an early onset autism without any history of regression: it means that all children displayed, from the beginning, the autistic symptoms constellation rated through the Behavioral Summarized Evaluation applied to the home movies of the first year of life (see Muratori et al., 2010 [25]). The children were recruited among those referred from multiple community sources to the the Scientific Institute "IRCCS Stella Maris", a suburban university hospital providing tertiary care to patients of all socioeconomic levels. The study has been approved by the Ethical Committee of

the Stella Maris Institute/University of Pisa, Italy. The Pisa HM data base includes children from biparental families with either typical or AD matched for gender and socio-economic status (all medium or good). Each child included in the Pisa HM data base had at least one scene from each of the first 3 semesters of life showing a situation in which social interaction could occur. Also, HM run for a minimum of 10 minutes for each of the first 3 semesters of life. The control group was recruited among children attending a local kindergarten attending a local kindergarten. It included 15 typically developing children (M/F ratio: 9/6) confirmed by non-pathological scores on the Child Behavior Check List [26]. After the automatic algorithm affective speech classification (step 4), the experimental group included 14 children (M/F ratio: 10/4) with a diagnosis of autism disorder (AD) without any sign of regression confirmed by the ADI-R. All AD children had a Childhood Autism Rating Scale (CARS) score >30. Mean
Intellectual Quotients (SD) were 72.86 (8.5). Detailed clinical data for each child are given in Table S1 (available online).

## Extraction of parent-infant interactions (Step 2)

An editor, blind to child diagnoses, selected all segments running for at least 40 seconds where the infant was visible and could be involved in human interaction from among the HMs of each child. Sequences with more than one adult interacting with the infant (aside from the adult holding the video camera) were excluded. For each infant, the sequences were organised in three periods of 6 months of age (≤6 month; 6–12 months; >12 months) labelled semester 1 (S1), semester 2 (S2) and semester 3 (S3), respectively. Sequences were randomly selected by group and by semester. Preliminary t-test analysis showed that the selected video material was comparable across groups and for each age range in length and number of human interactions [25]. The number of scenes per infant is given in second column of Table S2 (available online).

## Computer-based coding system (Step 3)

The Observer 4.0® was configured for the application of the Infant Caregiver Behavior Scale (ICBS) to the video file. The ICBS (Annex S1 available online) is composed of items assessing the ability of the infant to engage in interactions and items describing CG solicitation for attention or stimulation of the infant. All target behaviors were described as Events which take an instant of time. CG regulation up and CG regulation down were described as events that take a period of time and have a distinct start and end.

Four coders were trained to use the computer-based coding system until they achieved a satisfactory agreement (Cohen's Kappa ≥0.7). The interactions derived from the HM of the two groups of children (AD and TD) were mixed, and each one was rated by one trained coder who was blind to which group the child belonged. For a continuous verification of inter-rater agreement, 25% of interactions were randomised and rated by two coders independently. The final inter-rater reliability, calculated directly by the Observer, showed a satisfactory Cohen-κ mean value ranging from 0.75 to 0.77.

## Studying parental and parentese contributions to parents infant interactions (Step 4)

To extract the caregiver's vocalisations from the video segments, we performed a manual segmentation of parents' vocalisations with The Observer 4.0®. We used Sound Forge 9.0 to extract the vocal segments from each video sequence. Vocal segments that were presented with poor audio quality or were imperceptible to the ear were excluded. At this stage, we lost one child per group because of poor HM audio quality. Manual segmentation provided us with a database of speech segments separated by cases (AD, TD) and by semester (S1, S2 and S3). In addition, manual segmentation allowed us to identify the following: the number/frequency of vocal segments, the duration of segments in each sequence, and who was speaking to the child (i.e., mother, father, other CG). Detailed data regarding the number of parent, mother, and father vocalizations as well as infant responses per infant are given in Table S2.

The segments of speech were analysed using a computerised classifier for categorisation as 'parentese' or other speech'. Classification according to acoustic components was required, as the interaction database included only CG vocalisations addressed to the infant. Because the "manual" study of acoustic components of the voice takes a very long time [27] and only allows for the

study of very short voice segments, the use of such an algorithm made it possible to conduct an extensive study of HMs based on their acoustic characteristics.

The whole system was described by Mahdhaoui et al. [21]. Here, we briefly describe the key components of this automatic system. Using classification techniques that are often used in speech and speaker recognition (GMM, Gaussian Mixture Model, and K-nn, k-nearest neighbours), we developed a parentese detection system and first tested it on the mode dependence of the speaker. The fusion of features and classifiers was also investigated. Given that HM are not recorded by professionals and often contain adverse conditions (e.g., with regard to noise, the camera, or microphones), acoustic segmentation of HM shows that segmental features play a major role in robustness [28]. Consequently, the utterances were characterised by both segmental (Mel Frequency Cepstrum Coefficients) and supra-segmental (e.g., statistics with regard to fundamental frequency, energy, and duration) features. We showed that segmental features alone contained very useful information for discrimination between parentese and other speech, and the combination of segmental features with supra-segmental ones outperformed the supra-segmental features. However, according to our detection results, prosodic features were also very promising. Based on the previous two conclusions, we combined classifiers that used segmental features with classifiers that used supra-segmental features and found that this combination improved the performance of our parentese detector considerably. In its most effective configuration, the novel detector used only the GMM classifier for both segmental and supra-segmental features (M, number of Gaussians for the GMM Classifier: M = 12 and M = 15, respectively, and λ = weighting coefficient used in the equation fusion: λ = 0.4). Performance was as follow: accuracy = 87.5% (95%CI = 82.91–92.08%); Positive Predictive Value, PPV = 88.47% (95%CI = 83.03–95.18%); Negative Predictive Value, NPV = 86.41% (95%CI = 79.4–92.88%) [21]. We also investigated the performance of the detector with these fusion parameters in detecting parentese versus other speech (non-parentese) within a second set of 200 utterances (100 parentese vs. 100 other speech) that were blindly validated by two psycholinguists extracted from 10 randomly-selected home videos with 12 independent speakers (all mothers). Performances under speaker-independent conditions were as follows: accuracy = 82% (95%CI = 73.87–89.58%); PPV = 86.36% (95%CI = 66.52–89.48%); NPV = 77.55% (95%CI = 76.73–96.6%) [21]. For the purpose of the current study, which also aimed to explore parentese in fathers, we analysed 100 sequences from fathers (50 parentese vs. 50 other speech) that were blindly validated by two psycholinguists. The system's performance was good: accuracy = 74% (95%CI = 64.27–82.26%); PPV = 71.43% (95%CI = 57.79–82.70%); NPV = 77.27% (95%CI = 62.16–88.53%). This level of prediction made it suitable for further studies of home videos.

For the interaction analysis, we first fused video coding and acoustic analysis. The computer-based coding system (The Observer) provided ".txt" files with the description of ICBS behaviours based on time. Vocalisations analysed by the computerised system provided two new tags: parentese vocalisation or other speech. These tags were reintegrated to the txt file as CG "state events". To summarise, CGinfant interactive behaviours could now be examined by type of vocalisation (parentese vs. other speech), semester (S1, S2 or S3) and speaker (mother vs. father vs. other CG) in terms of frequency (number of events) and duration of CG vocalisations (in seconds).
## Creation of the interaction database (step 5)

We first created an interaction data base by extracting all child behaviors occurring within the 3 seconds following any caregiver behavior (including events that occur within the same second). The 3 second window was based on available literature on synchrony and previous work [14,15]. Extraction was performed using a Linux-based script. The sequence of n interactive patterns is termed n-gram as usually performed in natural language processing or gene analysis. In this study, we only focused on bigram modelling. Given the large number of possible types of interaction ([CG item × infant item]), and the low frequency of several items in the data base, we created five CG meta-behaviors (Vocal solicitation, Touching, Gestural solicitation, Regulation up, Regulation down) and six infant meta-behaviors (Behavior with object and 5 types of Behaviors with people: Vocalizations, Inter subjective behavior, Seeking people, Receptive to people, Orient- ing towards people,) by grouping ICBS items. Meta behaviors are shown in the left column of ICBS Grid and are based on previous studies [15,25] (Annex 1). Then, we repeated the process of extraction to obtain finally, for each standard situation, all sequences of CG meta-behavior and infant meta-behavior occurring within a 3-second time window.

## Quantitative statistics (Step 6)

Following this multivariate analysis with four fixed factors, we conducted two post-hoc multivariate analyses (also using GLMM and infant response following a parental vocalization as the dependent variable). The first post-hoc analysis investigated Semester, Speaker and Vocalisation Type as independent variables within the same Group and the second with just Speaker and Vocalisation Type as independent variables within each Group and Semester category, still considering subjects as a random effect. We used a two-tailed threshold of significance for each calculation of p, and p = .05 was the level of significance.

## Results

### Parentese in the HM by group

We first explored, as a whole, before the interactive database extraction (step 5), the proportion of parentese in parents' vocalisation and in parents' soliciting behaviour (called Regulation Up in the ICBS) by group (figure 2A). As shown in figure 2A, we did not find any differences between groups for parents' vocalisation. The proportion of parentese was higher in mother vocalisations (40 to 60% of parentese) than father vocalisations (15 to 20% of parentese). Use of parentese among mothers showed the same decrease over time in both groups ($\beta$ = -0.51; standard error = 0.097; p = <10⁻⁶; $\beta$ = -0.55; std error = 0.11; p = <10⁻⁶ for S2 vs. S1, and S3 vs. S2, respectively). Parentese among fathers significantly decreased between S1 and S2 ($\beta$ = -0.4; std error = 0.165; p = 0.015) but not between S2 and S3 ($\beta$ = -0.29; std error = 0.178; p = 0.108) in both groups. Fathers of AD children tended to use more parentese than those of TD children ($\beta$ = 0.6502; std error = 0.3355; p = 0.052) and also assumed a greater part in vocalizations (either using parentese or other speech) addressed to infants ($\beta$ = 0.794; std error = 0.3752; p = 0.03). In other words, fathers of AD children spoke to their infants more than fathers of TD children regardless of whether they used affective speech. Regarding parents Regulation Up (figure 2B), we found that these parents soliciting behaviors were “full” of parentese, nearly doubling the proportion of parentese found in all vocalizations in both groups and at all 3 semesters (40 to 70% vs. 20 to 40% of parentese in parents Regulation Up and parents all vocalizations, respectively).

## Infant response to parents' vocalisation by time, group, parent's gender and acoustic characteristics

Table 1 shows the number of parental vocalizations and the overall number of infant responses following parental vocalizations as well as the number of infant responses according to subtype (e.g., towards an object in comparison to towards people) for each semester. The GLMM analysis is summarised in table 2. Considering any infant meta-behaviors that were a response to each parent's vocalization within a 3-second time window (parentinfant interaction), the probability of infant responses increased significantly between the first and the second semester and then remained stable in quantity. However, they significantly changed in terms of quality of response: between S2 and S3, the probability of infant responses to parental vocalizations that involved orientation “towards an object” increased, whereas infant responses to parental vocalizations that involved orientation “towards people” decreased. Finally, the probability of infant intersubjective responses showed a continuous increase from S1 to S3. When considering the AD compared with TD group, we found that infants who later developed AD had fewer overall responses, specifically fewer responses to parental vocalizations that involved orientation “towards people” and less intersubjective behaviour. Post-hoc analyses conducted by semester showed that this lower rate of response to parents’ vocalization was significant for AD infants as early as the first semester ($\beta$ = -0.52; std error = 0.2613; p = 0.04).

Although mothers vs. fathers did not differ in the number of responses they induced in their infant, mothers appeared to be significantly associated with infant expressive responses, whereas fathers were significantly associated with infant intersubjective behaviors (table 1). In particular, post-hoc analysis conducted on the AD group showed a significant association between fathers' vocalizations and both the intersubjective responses ($\beta$ = 1.038; std error = 0.3702; p = .005) and active behavior (seeking people) during the third semester ($\beta$ = -0.823; std error = 0.3676; p = .02).

Finally, as opposed to other speech, parentese (produced by the mother or the father) was also significantly associated with infant responses as a whole, infant responses involving orientation towards people and infant receptive responses (table 1). In particular, post-hoc analyses conducted on the AD group showed that parentese addressed to infants who will later develop autism was significantly associated with infant responses involving orientation towards people ($\beta$ = 0.228; std error = 0.10188; p = .02) and infant receptive behaviours ($\beta$ = 0.51610; std error = 0.15245; p = .0007); we also found that parentese addressed to infants who will later develop autism tended to be associated with infant expressive behaviours (e.g., vocal response) ($\beta$ = 0.2401; std error = 0.1242; p = 0.05). When considering parentese facilitation of infant responses by semester, we found that parentese facilitation of infant response towards people ($\beta$ = 0.6027; std error = 0.2150; p = 0.005) and infant receptive behaviours ($\beta$ = 0.7640; std error = 0.2926; p = 0.009) appears as early as the first six months of life for infants with AD.

## Discussion

The use of engineering methods related to social signal processing allowed a focus on dynamic parent→infant interaction instead of single behaviors of the baby or parent. It allowed us: (i) to focus on antecedents and consequences of interactive behaviours; (ii) to note significant sequences that could prompt or inhibit social interaction in a naturalistic way; (iii) to specifically study acoustic components of prosody, such as parentese, a key moderator of early interaction [8]. Our results regarding the
<figure><img src="image_4.png" /><figcaption>**Figure 2.** Proportion of parentese based on acoustic characteristics in mothers' and fathers' vocalisation of TD infants or infants with AD (2A); in caregiver Regulation Up and all vocalisation whether the infant had TD or AD (2B). TD = Typical Development; AD = Autism Disorder; CG = Care Giver; Reg Up = Regulation Up; All voc = All vocalisations. doi:10.1371/journal.pone.0061402.g002</figcaption></figure>

facilitating effects of parentese on TD are concordant with the literature in which parentese is known to capture an infant's attention and elicit an infant's engagement. Concordant with this definition, in our study, parentese was significantly associated with "receptive" responses (looking at people, smiling at people, enjoying being with people and syntony). We discuss our results separately with regard to our initial hypotheses on children with AD, Dean Falk's theory of prelinguistic evolution in early hominins, and possible therapeutic implications in the early treatment of autism.

## Are the current results supporting our hypotheses?

We first hypothesised that parentese towards children with AD should decrease over time and that this decrease will likely be greater than that observed in parentese towards TD children. The results presented here did not support H1. We can interpret this result with at least three alternative explanations: (i) the 6-month time windows we used are too long to measure any differences in slope; (ii) TD infants are so interactive [15] that their parents do not need, after S2, to use parentese for successful interactions; or (iii) parents of AD infants use more parentese because they sense the on-going pathologic process. This third hypothesis is congruent with our previous results of an increasing of Regulation Up among CGs of infants with autism [15], as Regulation Up is "full" of parentese (figure 2B). A TD twin case study also has shown that a twin's mother used more parentese with the twin who was less reactive [30]. By suggesting that parents feel the pathological process ongoing, we want to guard against the idea that the parenting behaviors are impaired and cause autism. In fact, when parents respond to their infant they behave as parents of TD infant [15]. Rather, we suggest that they are some sort of reaction to early sign that are implicitly perceived by the parents. Although H1 is not supported, the lack of reciprocity from the AD infant could modify interaction dynamics, however, as we found that AD fathers were significantly more involved in interactions than TD fathers, particularly after one year. The importance of reciprocity and synchrony in early parent-infant interaction [14] was already supported in developmental studies of premature babies [31], in cases of parents being stressed during pregnancy [32] and in cases

of parents with a previous history of a child with AD [33]. In the current study, parents, particularly fathers, did not receive any diagnosis but changed their behaviour to adapt to the lack of reciprocity. This behavioural change will be called father's involvement in interacting with infants, hereafter.

The second hypothesis (H2) proposed that AD infants should be capable of interacting with and responding to parentese from a very early age. The results presented here support H2, as we found that parentese (produced by the mother or the father) appeared to be significantly associated with infant responses as a whole and with infant responses involving orientation towards people. This was also the case for infants who will later develop AD. This finding may have promising therapeutic implications (see below).

## Implication for Dean Falk's theory regarding pre-linguistic evolution in early hominins

Falk's theory regarding pre-linguistic evolution in early hominins is based on a comparison of mother-infant gestural and vocal interactions in chimpanzees and humans [34]. She noted that pre-linguistic vocal substrates that had prosodic features similar to contemporary parentese evolved with the trend regarding enlarging brains in late australopithecines/early Homo. This progressively increased the difficulty of parturition, causing a selective shift towards females that gave birth to relatively undeveloped neonates. In contrast to chimps, which favour physical contact with their infants that are mature enough to grasp his/her mother, Falk hypothesised that in humans, (i) mothers adopted new foraging strategies that entailed maternal silencing, reassuring, and controlling of the behaviours of physically removed infants, (ii) the meanings of certain utterances (words) became conventionalised as mothers increasingly used prosodic and gestural markings to encourage juveniles to behave and obey. This hypothesis is based on the premises thatominin mothers that attended vigilantly to infants were strongly selected for and that such mothers had genetically based potentials for consciously modifying vocalizations and gestures to control infants, both of which receive support from the literature [19,35–37]. Regarding human early interaction, this theory proposes touching, grasping, and skin-to-skin contact as old evolutionary moderators and
<table><caption>**Table 1.** Number of parental vocalizations and number of total infant responses and infant responses according to subtype per semester.</caption><thead><tr><th rowspan="2">Parental vocalizations</th><th rowspan="2">Total infant responses</th><th colspan="2">2 types of infant responses</th><th colspan="2">5 categories of responses toward people</th><th rowspan="2">Active responses</th><th rowspan="2">Exploratory responses</th><th rowspan="2">Inter-subjective responses</th></tr><tr><th>Toward object</th><th>Toward people</th><th>Receptive responses</th><th>Expressive responses</th></tr></thead><tbody><tr><td colspan="9">INFANT WHO WILL LATER DEVELOP AUTISM (N = 14)</td></tr><tr><td>S1</td><td>652</td><td>315</td><td>44</td><td>271</td><td>88</td><td>128</td><td>13</td><td>32</td><td>10</td></tr><tr><td>S2</td><td>983</td><td>619</td><td>116</td><td>503</td><td>121</td><td>217</td><td>35</td><td>88</td><td>42</td></tr><tr><td>S3</td><td>672</td><td>418</td><td>127</td><td>291</td><td>44</td><td>102</td><td>49</td><td>42</td><td>54</td></tr><tr><td colspan="9">INFANT WITH TYPICAL DEVELOPMENT (N = 14)</td></tr><tr><td>S1</td><td>950</td><td>578</td><td>115</td><td>463</td><td>126</td><td>229</td><td>27</td><td>57</td><td>24</td></tr><tr><td>S2</td><td>1170</td><td>824</td><td>167</td><td>657</td><td>154</td><td>253</td><td>60</td><td>76</td><td>114</td></tr><tr><td>S3</td><td>769</td><td>530</td><td>146</td><td>384</td><td>32</td><td>155</td><td>30</td><td>31</td><td>136</td></tr></tbody></table>

S= Semester 1, 2, 3.
doi:10.1371/journal.pone.0061402.t001

<table><caption>**Table 2.** Infant response to caregiver vocalisation by time, group, parent's gender (mother vs. father) and acoustic characteristics (parentese vs. other speech) in home movies from infants who will later develop autism (N = 14) versus typically developing infants (N = 14).</caption><thead><tr><th>Variable</th><th>All infant responses</th><th>Toward people</th><th>Toward object</th><th>Receptive responses</th><th>Expressive responses</th><th>Exploratory responses</th><th>Inter-subjective responses</th><th>Active responses</th></tr></thead><tbody><tr><td>Sem 2 vs. Sem 1</td><td>β=0.52 SE=0.07351 (p&lt;10<sup>-11</sup>)</td><td>β=0.34 SE=0.07171 (p&lt;10<sup>-5</sup>)</td><td>β=0.36 SE=0.11302 (p=.001)</td><td>β=-0.02 SE=0.10564 (ns)</td><td>β=-0.01 SE=0.0857 (ns)</td><td>β=0.23 SE=0.1447 (ns)</td><td>β=1.39 SE=0.2004 (p&lt;10<sup>-11</sup>)</td><td>β=0.53 SE=0.2020 (p=.007)</td></tr><tr><td>Sem 3 vs. Sem 2</td><td>β=0.01 SE=0.0789 (ns)</td><td>β=-0.21 SE=0.0751 (p&lt;10<sup>-4</sup>)</td><td>β=0.40 SE=0.103 (p&lt;10<sup>-4</sup>)</td><td>β=-0.84 SE=0.14305 (p&lt;10<sup>-8</sup>)</td><td>β=-0.15 SE=0.0942 (ns)</td><td>β=-0.39 SE=0.1574 (p=.01)</td><td>β=0.54 SE=0.1299 (p&lt;10<sup>-4</sup>)</td><td>β=0.17 SE=0.17337 (ns)</td></tr><tr><td>AD vs. TD</td><td>β=-0.48 SE=0.1510AD&lt;TD (p=.001)</td><td>β=-0.39 SE=0.1694 AD&lt;TD (p=.01)</td><td>β=-0.13 SE=0.2336 (ns)</td><td>β=-0.18 SE=0.2789 (ns)</td><td>β=-0.40 SE=0.2325 (ns)</td><td>β=0.28 SE=0.2382 (ns)</td><td>β=-0.87 SE=0.3161 AD&lt;TD (p=.005)</td><td>β=0.03 SE=0.3179 (ns)</td></tr><tr><td>Mother vs. Father</td><td>β=0.08 SE=0.0665 (ns)</td><td>β=0.11 SE=0.0643 (ns)</td><td>β=-0.07 SE=0.0928 (ns)</td><td>β=-0.11 SE=0.1053 (ns)</td><td>β=0.23 SE=0.0801 (p=.004)</td><td>M&gt;F</td><td>β=0.16 SE=0.1296 (ns)</td><td>β=-0.24 SE=0.1237 M&lt;F (p=.04)</td></tr><tr><td>Parentese vs. Other speech</td><td>β=0.16 SE=0.0703 p<sub>est</sub>&gt;OS (p=.02)</td><td>β=0.17 SE=0.0672 p<sub>est</sub>&gt;OS (p=.007)</td><td>β=-0.07 SE=0.1004 (ns)</td><td>β=0.52 SE=0.1024 p<sub>est</sub>&gt;OS (p=10<sup>-6</sup>)</td><td>β=0.09 SE=0.0803 (ns)</td><td></td><td>β=-0.10 SE=0.1373 (ns)</td><td>β=-0.23 SE=0.1453 (ns)</td></tr></tbody></table>

M= mother; F=father; P<sub>est</sub>= Parentese; OS= other speech; AD= autism disorder; TD= typical development; SE= Standard Error; ns= non significant.
doi:10.1371/journal.pone.0061402.t002
parentese, gesturing, and infant crying as recent evolutionary
moderators. Parents of infants who will develop AD change their
interactive pattern of behaviour by recruiting both moderators
 touching [15], as well as parentese and father involvement in
 interacting with infants [current results] for interacting with their
 infants. These behaviours were found to be adaptive, and thus, the
 findings support Falk's theory. Although father involvement in
 interacting with infants is not discussed *per se* in Falk's theory,
 triadic interaction (involving baby, mother and father) may be
 specific to human social and family behaviors [38]. Although this
 field has been scarcely investigated, recent studies support the role
 of father in early interaction both at behavioural [39] and
 biological levels [40]. Figure 3 summarises, in infants who will later
develop autism, the pathologic trajectory of infant behaviors and
 the changes in CG stimulations to adapt to their infant.

Clinical implication for early treatment of autism

To our knowledge, the current study is the first to suggest that parentese is significantly associated with infant responses towards people in infants who later develop AD. For TD children, parentese seems to mediate (and also reflect) an interactive loop between the infant and his/her caregiver in which each partner's response may increase, in turn, the stimulation by the other partner. Moreover, this interactive loop (at the behavioural level) is underpinned by the emotional charge (at the affective level) and impacts attention, learning and the construction of intersubjective tools, such as joint attention and communicative skills (at the cognitive level) [18,19]. Direct evidence for the interaction of cognitive and social levels is offered by Kuhl's finding that infant's learning of the phonetic properties of a language requires interaction with a live linguistic partner [41]. Audio-visual input

alone is not sufficient. However, we were unable to find any study
comparing interest in parentese versus other speech in children
with autism. We know that (i) children with AD can process some
aspects of human voices [42], although they display no specific
cortical activation in response to human voices [43]; (ii) they do
not show the expected preference for their mother's speech [44];
(iii) joint attention and immediate imitation appear to be
important for setting the stage for early language acquisition in
AD while representational skills (toy play, deferred attention)
contribute to the expansion of communication skills [45]; (iv) also,
children with AD fail to orient to naturally occurring social stimuli
such as name called and hand clapping [46].

The results of the current study support the view that parentese,
an early naturally occurring social stimulus, might provide useful
feedback during social interaction sessions, particularly for very
young children. Preliminary data support this view: (i) social and
linguistic processing of speech in preschool children with autism
could be correlated with behavioral and electrophysiological
measures [47]; (ii) predictive correlations between attention to
child directed speech (which is generally rich in parentese) and
receptive language abilities were found in ASD [48,49]; (iii) young
ASD children showed less sustained attention to child directed
speech performed by an actor compared to typically developing
peers matched for chronological age. They did not, however, look
less overall to child directed speech stimuli than typically
developing peers matched for language age [50]; (iv) in a single
case exploratory study, Laznik et al. observed HM sequences in
which a withdrawn infant who will later develop autism suddenly
appears joyful when the parent implements a vocal expression
using parentese [27]. We now aim to explore the use of a parentese
biofeedback loop based on our algorithm [21] to improve the

<figure><img src="image_5.png" /></figure>

**Figure 3. Infants who will later develop autism: pathologic trajectory of infant's behaviours and changes in parents' stimulation to adapt to their infant.** In this figure, we summarised early interaction between infants who will subsequently develop autism and their parents. Infants show less intersubjective behaviours and orienting towards people<sup>o</sup>. Parents adapt their behaviour by using more regulation up<sup>o</sup> and touching<sup>o</sup> [13]. Regulation Up/Down is defined as caregiver vocalisation that modulates the child's arousal and mood, to either excite (reg-up) or calm (reg-down). Regulation up is full of parentese<sup>o</sup>, and this specific prosody appears to be significantly associated with the overall level of infants' responses, specifically infants' responses to parental vocalizations involving orientation towards people and receptive behaviours<sup>o</sup>. At the third semester (S3), compared to typically developing children, fathers of infants who will later develop autism appear to commit themselves more<sup>o</sup> and the vocalisations of fathers of children with AD are significantly associated with infant's intersubjective responses and seeking people<sup>o</sup>. doi:10.1371/journal.pone.0061402.g003
emotional balance of CG prosody in the context of therapeutic interactive sessions (FP7 MICHELANGELO Project) and to assess whether parentese-like prosody is associated with better social interaction.

## Limits and strengths of this study

The first limitation is the sample size. Because we used rigorous statistical methods that took into account the random subject effect and autocorrelation, and because scenes were highly variable for a given infant (due to the great variability among scenes), some strong tendencies did not reach statistical significance. A larger sample would most likely have allowed us more analysable and/or significant results. Second, HM are not standardised, and analyses are retrospective from the time of positive diagnosis. Current research prefers prospective follow-up of high risk samples (e.g., siblings of AD children) with experimental procedures to assess early infant-parent interaction despite the fact that parents are aware of the risk. Recently, the British Autism Study of Infants' Siblings reported that early dyadic interaction between at-risk infants and their parents was associated with later diagnosis of autism [51]. This result is consistent with ours. Third, despite previous works with another pathologic group (infants who will develop intellectual disability without symptoms of AD), we were not able to include HM from this group in the current study, as the much lower occurrence of interaction, CG vocalisation and infant meta-behaviors prevented any statistical analysis [15]. However, to explore whether the severity of autism or comorbid ID significantly biased the current results, we performed a GLMM analysis with semester, speaker, type of speech, IQ and CARS score as the independent variables and infant response following a parental vocalization as the dependent variable. IQ and CARS scores showed no significant association with infant responses (data not shown). Finally, we modelled parent-child interactions as synchronous CGxInfant events using an approximation: CG vocalization followed by an infant response in a 3-second time window. However, this model is not similar to naturalistic observations, which take into account longer lasting periods of time and more continuous series of events (e.g., latency response measures, cross recurrence analysis, and slope analysis) [52,53]. Strengths of the study include the spontaneous adaptation to the pathologic process that is observable in HM compared to the study of infant-parent interaction in the case of studies with ASD siblings [33] or to more experimental settings. Indeed, Wan et al. [33] suggested that infant

siblings at risk of autism were exposed to a more directive parental interactive style relatively early in infancy. Second, the use of an automatic detector of acoustic components in prosody related to emotion [21] helped us in distinguishing infant-directed speech with parentese prosody versus infant-directed speech without such prosody. Third, we were able to distinguish between mother versus father, which allowed the assessment of both dyadic and triadic dynamics [54]. Fourth, despite its size, the group of patients was quite homogeneous because of rigorous exclusion criteria used in the Pisa HM data base.

## Conclusion

Parents of infants who will develop autism change their interactive pattern of behaviour, increasing both parentese prosody and father's involvement in interacting with infants; both are significantly associated with infant's social responses. We stress the possible therapeutic implications of these findings.

## Supporting Information

<caption>**Table S1** Clinical characteristics of each infant included in the AD group (N = 14).</caption>

(DOC)

<caption>**Table S2** Number of scenes, parental vocalizations, maternal vocalizations, paternal vocalizations and infant responses per infant.</caption>

(DOC)

<caption>**Annex S1** Infant's and caregiver's behaviors and meta-behaviors from the infant caregiver behavior scale (ICSB).</caption>

(DOC)

## Acknowledgments

The authors thank A Meltzoff for critical discussion and reading of the manuscript.

## Author Contributions

Conceived and designed the experiments: DC MC FM MCL SM. Performed the experiments: FA PM SM AM CSG RC. Analyzed the data: CSG AM MC DC. Contributed reagents/materials/analysis tools: AM MC. Wrote the paper: DC RC CSG AM MCL FA PM SM FM MC.

## References

1. Stone W, Hoffman EL, Lewis S, Ousley O (1994) Early recognition of autism: Parental reports vs. clinical observation. Arch Paediatrics Adolesc Med 148:174-9.

2. Saint-Georges C, Cassel RS, Cohen D, Chetouani M, Laznik MC, et al. (2010) What studies of family home movies can teach us about autistic infants: A literature review. Res Autism Spectr Disord 4(3):355-66.

3. Werner E, Dawson G, Osterling J, Dinno N (2000): Brief report: Recognition of autism spectrum disorder before one year of age: A retrospective study based on home videotapes. J Autism Dev Disord 30(2):157-62.

4. Guinchat V, Chamak B, Bonniau B, Bodeau N, Perisse D, et al. (2012) Very early signs of autism reported by parents include many concerns not specific to autism criteria. Res Autism Spectr Disord 6: 589-601.

5. Zwaigenbaum L, Bryson S, Rogers T, Roberts W, Brian J, et al. (2005) Behavioral manifestations of autism in the first year of life. Int J Dev Neurosci 23(2-3):143-52.

6. Elsabbagh M, Johnson MH (2010) Getting answers from babies about autism. Trends Cogn Sci 14(2):81-7.

7. Meltzoff AN, Kuhl PK, Movellan J, Sejnowski TJ (2009) Foundations for a new science of learning. Science 325: 284-288.

8. Kuhl PK (2004) Early language acquisition: Cracking the speech code. Nature Rev Neuroscience 5: 831-843.

9. Goldstein MH, King AP, West MJ (2003) Social interaction shapes babbling: testing parallels between birdsong and speech. PNAS 100: 8030-8035.

10. Chaby L, Chetouani M, Plaza M, Cohen D (2012) Exploring multimodal social-emotional behaviors in autism spectrum disorders. Workshop on Wide Spectrum Social Signal Processing, ASE/IEEE International Conference on Social Computing. Pages 950-954.

11. Delaherche E, Chetouani M, Mahdhaoui A, Saint-Georges C, Viaux S, et al. (2012) Interpersonal synchrony: a survey of evaluation methods across disciplines. IEEE Trans Affect Comput 3: 349-365.

12. Stormark KM, Braarud HC (2004) Infants' sensitivity to social contingency: a "double video" study of face-to-face communication between 2-and 4-month-olds and their mothers. Infant Behav Dev 27(2):195-203.

13. Crown CL, Feldstein S, Jasnow MD, Beebe B, Jaffe J (2002) The cross-modal coordination of interpersonal timing: Six-week-olds infants' gaze with adults' vocal behavior. J Psycholinguistic Res 31(1):1-23.

14. Feldman R (2007) Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J Child Psychol Psychiatry 48(3-4):329-54.

15. Saint-Georges C, Mahdhaoui A, Chetouani M, Cassel R, Laznik M-C, et al. (2011) Do parents recognize autistic deviant behavior long before diagnosis? Taking into account interaction using computational methods. Plos One 6(7): e22393.

16. Fernald A, Kuhl P (1987) Acoustic determinants of infant preference for motherese speech. Infant Behav Dev 10(3):279-93.

17. Hirsh-Pasek K, Kemler Nelson DG, Jusczyk PW, Cassidy KW (1987) Clauses are perceptual units for young infants. Cognition 26(3):269-86.
18. Braarud HC, Stormark KM (2008) Prosodic modification and vocal adjustments in mothers' speech during face-to-face interaction with their two- to four-month-old infants: A double video study. Social Dev 17(4):1074-84.

19. Falk D (2009) Findings our tongues: mothers, infants and the origin of languag (Basic Books, New York)

20. Grossmann T, Oberecker R, Koch SP, Friederici AD (2010) The Developmen- tal Origins of Voice Processing in the Human Brain. Neuron 65: 852-858.

21. Mahdhaoui A, Chetouani M, Cassel RS, Saint-Georges C, Parlato E, et al. (2011) Computerized home video detection for motherese may help to study impaired interaction between infants who become autistic and their parents. Inter J Methods Psychiatr Res 20(1):e6-e18.

22. Cassel RS, Saint-Georges C, Mahdhaoui A, Chetouani M, Laznik MC, et al. (in press) Course of maternal prosodic incitation (motherese) during early development in autism: an exploratory home movie study. Interaction Studies.

23. Rutter M, Le Couteur A, Lord C,editors (2003) ADI-R: the autism diagnostic interview-revised. (Western Psychological Services, Los Angeles, CA)

24. Schopler E, Reichler RJ, Renner BR, editors (1998) The Childhood Autism Rating Scale.(Western Psychological Services, Los Angeles)

25. Muratori F, Apicella F, Muratori P, Maestro S (2010) Intersubjective disruptions and caregiver-infant interaction in early Autistic Disorder. Res Autism Spectr Disord 5(1):408-17.

26. Achenbach TM, Rescorla L, editors (2000) Manual for the ASEBA Preschool Forms and Profile.(ASEBA, Burlington, VT)

27. Laznik M, Maestro S, Muratori F, Parlato E (2005) Les interactions sonores entre les bébés devenus autistes et leurs parents. In: M-F Catarède GK, editor. Au commencement était la voix (Erès, Paris)

28. Schuller B, Batliner A, Seppi D, Steidl S, Vogt T, et al (2007) The relevance of feature type for the automatic classification of emotional user states: low level descriptors and functionals. Proceedings of InterSpeech

29. Cnann A, Laird N, Slasor P (1997) Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Statist Med 16:2349-80.

30. Niwano K, Sugai K (2003) Maternal accommodation in infant-directed speech during mother's and twin-infants' vocal interactions. Psychol Rep 92(2):481-7.

31. Feldman R (2006) From biological rhythms to social rhythms: Physiological precursors of mother-infant synchrony. Dev Psychol 42(1):175-88.

32. Viaux-Savelon S, Dommergues M, Rosenblum O, Bodeau N, Aidane E, et al. (2012) Prenatal Ultrasound Screening: False Positive Soft Markers May Alter Maternal Representations and Mother-Infant Interaction. PloS One 7:(1) e30935.

33. Wan MW, Green J, Elsabbagh M, Johnson M, Charman T, et al. (2012) Parent- infant interaction in infant siblings at risk of autism. Res Autism Spectr Disord 33(3):924-32.

34. Falk D (2004) Prelinguistic evolution in early hominins: whence motherese? Behav Brain Sci 27(4):491-503; discussion -83.

35. Bickerton D (2002) Foraging Versus Social Intelligence in the Evolution of Protolanguage. The Transition to Language. 207-25. In A. Wray, editor, The transition to language. (Oxford University Press, Oxford)

36. Plooy FX (1984) The behavioral development of free-living chimpanzee babies and infants (Ablex Pub. Corp., Norwood, N.J.)

37. Small M (1998) Our Babies, ourselves: how biology and culture shape the way we parent (Anchor Books, Doubleday)

38. Groenen M (1996) Leroi-Gourhan: essence et contingence dans la destinée humaine.(De Boeck Université, Bruxelles)

39. Ramchandani P, Domoney J, Sethna V, Psychogiou L, Vlachos H, et al. (2012) Do early father-infant interactions predict the onset of externalising behaviours in young children? Findings from a longitudinal cohort study. J Child Psychol Psychiatry online first DOI: 10.1111/j.1469-7610.2012.02583.x

40. Atzil S, Hendler T, Zagoory-Sharon O, Winetraub Y, Feldman R (2012) Synchrony and Specificity in the Maternal and the Paternal Brain: Relations to Oxytocin and Vasopressin. J Am Acad Child Adol Psychiatry 51: 798-811.

41. Kuhl PK, Tsao FM, Liu HM (2003) Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proc Natl Acad Sci U S A. United States 100(15): 9096-101.

42. Groen WB, van Orsouw L, Zwiers M, Swinkels S, van der Gaag RJ, et al. (2008) Gender in voice perception in autism. J Autism Dev Disord 38(10):1819-26.

43. Boddaert N, Chabane N, Belin P, Bourgeois M, Royer V, et al. (2004) Perception of complex sounds in autism: abnormal auditory cortical processing in children. Am J Psychiatry 161(11):2117-20.

44. Klin A (1991) Young autistic children's listening preferences in regard to speech: a possible characterization of the symptom of social withdrawal. J Autism Dev Disord 21(1):29-42.

45. Toth K, Munson J, Meltzoff AN, Dawson G (2006) Early predictors of communication development in young children with autism spectrum disorder: joint attention, imitation and toy play. J Autism Dev Disord 36: 993-1005.

46. Dawson G, Meltzoff AN, Osterling J, Rinaldi J, Brown E (1998) Children with autism fail to orient to naturally occurring social stimuli. J Autism Dev Disord 28: 479-485.

47. Kuhl PK, Coffey-Corina S, Padden D, Dawson G (2005) Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. Dev Sci 8(1):F1-F12.

48. Paul R, Chawarska K, Fowler C, Cicchetti D, Volkmar F (2007) "Listen my children and you shall hear": Auditory preferences in toddlers with autism spectrum disorders. J Speech Language Hearing Res 50: 1350-1364.

49. Watson LR, Baranek GT, Roberts JE, David FJ, Perryman TY (2010) Behavioral and physiological responses to child-directed speech as predictors of communication outcomes in children with autism spectrum disorders. J Speech Language Hearing Res 53: 1052-1064.

50. Watson LR, Roberts JE, Baranek GT, Mandulak KC, Dalton KC (2012) Behavioral and Physiological Responses to Child-Directed Speech of Children with Autism Spectrum Disorders or Typical Development. J Autism Dev Disord 42:1616-1629.

51. Wan MW, Green J, Elsabbagh M, Johnson M, Charman T, et al. (2012) quality of interaction between at-risk infants and caregiver at 12-15 months is associated with 3-year autism outcome. J Child Psychol Psychiatry. Doi:10.1111/ jcpp.12032.

52. Warlaumont AS, Oller DK, Dale R, Richards JA, Gilkerson J, et al. (2009) Proceeding 32d Annual Conference of the Cognitive Science Society. The Cognitive Science Society Publisher, pages: 121-126.

53. Goldstein MH, Schwade JA, Bornstein MH (2009) The value of vocalizing: five-month-old infants associate their own non cry vocalizations with responses from caregivers. Child Dev 80: 636-644.

54. Fivaz-Depeursinge E, Frascarolo F, Corboz-Warnery A (1996) Assessing the triadic alliance between fathers, mothers, and infants at play. New Directions for Child and Adolescent Development (74):27-44.