Exp Brain Res (2008) 184:599–603 DOI 10.1007/s00221-007-1256-x R ES EA R C H N O T E Manual actions aVect vocalizations of infants Paolo Bernardis · Arianna Bello · Paola Pettenati · Silvia Stefanini · Maurizio Gentilucci Received: 14 June 2007 / Accepted: 12 December 2007 / Published online: 9 January 2008 © Springer-Verlag 2007 Abstract Upper limb gestures, as well as transitive actions (i.e. acted upon an object) when either executed or observed aVect speech. Broca’s area seems to be involved in integration between the two motor representations of arm and mouth (Bernardis and Gentilucci, Neuropsychologia, 44:178–190, 2006, Gentilucci et al., Eur J Neurosci, 19:190–202, 2004a, Neuropsychologia, 42:1554–1567, 2004b, J Cogn Neurosci, 18:1059–1074, 2006). The relevance of these data is in relation with the hypothesis that language evolved from manual gestures, and was gradually transformed in speech by means of a system of dual motor commands to hand and mouth (Gentilucci and Corballis, Neurosci Biobehav, Rev 30:949–960, 2006). The present study aimed to verify whether this system of integration between gestures (and transitive actions) and speech is involved also in the language development of infants. Vocalizations of infants aged between 11 and 13 months were recorded during both manipulation of objects of diVerent size and request arm gestures towards the same objects presented by the experimenter. Frequency in voice spectra increased when the infants manipulated or gestured to large objects in comparison with the same activities directed to small objects. These data suggest that intrinsic properties of an object evoking commands of manual interaction are used to identify that object, and to communicate. P. Bernardis · A. Bello · P. Pettenati · S. Stefanini · M. Gentilucci (&) Dipartimento di Neuroscienze, Università di Parma, Via Volturno 39, 43100 Parma, Italy e-mail: [email protected] A. Bello · P. Pettenati · S. Stefanini Centro Studi sullo Sviluppo Motorio e Linguistico del Bambino, Università di Parma, Via Volturno 39, 43100 Parma, Italy Keywords Hand–arm action · Gesture · Speech · Voice formants · Infants · Language development Introduction The origin of human language continues to pose a major challenge to contemporary neuroscience. In one view, spoken language might have evolved from a communication system employing manual gestures (Corballis 2002; Gentilucci and Corballis 2006; Hewes 1973; Rizzolatti and Arbib 1998). This hypothesis is primarily supported by the discovery of two classes of neurons in monkey premotor cortex. The Wrst class discharges when the animal executes a manual action as well as it observes the same action (i.e. the grasp) performed by another individual (Gallese et al. 1996). During evolution this mirror system might have acquired the function of interpreting and sending messages with the arm (Rizzolatti and Arbib 1998). The second class discharges when the same action (i.e. the grasp) is performed with the arm or the mouth (Rizzolatti et al. 1988). This system established initially in the context of the acts of grasp and ingestive movements, adapted later for communication. In other words it may form the basis for the transfer of a communication system from hand to mouth. By means of the mirror system, humans can understand action meaning by activating the motor representation of the observed action and might have used this gesture repertoire to exchange information. Using the dual hand-mouth command system this arm gesture repertoire could be shared with and transferred to the mouth (Gentilucci and Corballis 2006). EVects of these two systems have been observed in modern humans. Indeed, it was found that the execution and the observation of the grasp of objects inXuence the simultaneous pronunciation of syllables 123 600 (Gentilucci 2003; Gentilucci et al. 2001; Gentilucci et al. 2004b). SpeciWcally, when executing or observing the grasp of large as compared to small objects the lip opening and formant 1 (F1) in the voice spectra increased, corresponding to variation in Wnger shaping during these grasp movements (Gentilucci 2003; Gentilucci et al. 2001; Gentilucci et al. 2004b). These eVects were not restricted to the grasp action. Indeed, also the execution/observation of the action of bringing large and small fruits to the mouth aVected the simultaneous pronunciation of syllables. The execution/observation of the action guided by large fruits induced an increase in formant 2 (F2) in comparison with the execution/observation of the same action guided by small fruits (Gentilucci et al. 2004a,b). Gentilucci and colleagues (Gentilucci et al. 2004b) discovered that the eVects of observation/execution of transitive actions on speech were greater in children (6–7 years aged) than in adults. On the basis of this result, we hypothesized that the activity of the mirror and the dual hand– mouth command systems could be involved in the Wrst stage of language development. This is in accordance with the evidence that a strict relationship exists between early speech development in children and several aspects of manual activity. For example, canonical babbling in infants aged 6–8 months is generally accompanied by rhythmic hand movements (Iverson and Thelen 1999). In addition, spoken language and manual gesture develop in parallel during the following stages of communicative and linguistic acquisition. Between 8 and 11 months, typically developing infants start to show systematic evidence of word comprehension (Caselli et al. 1995). This phenomenon is correlated with increasing capacity to execute explorative and manipulative play with objects and with the emergence of deictic gestures (request, giving, showing, declarative pointing), that precede and accompany the appearance of the Wrst words (Volterra et al. 2005; Bates and Dick 2002). The deictic gestures are used to draw attention to objects, locations or events (Capirci et al. 2005). The infant’s communicative intent to request is conveyed by request (hand with opened Wngers) or pointing gestures. Frequently, request gestures are accompanied by vocalizations (Bates 1976): Pizzuto et al. (2005) found that these vocalizations are temporally coordinated with gesture execution. However, up to now the functional relationships between these vocalizations and gestures have not been investigated. Summing up, language development seems to be more strictly related to manual activity mainly in the age approximately between 8 and 13 months, i.e. before and at the beginning of verbal production. At this age infants become able to use appropriately the objects and to execute deictic gestures in order to communicate their requests. The hypothesis that manual interactions with objects contribute to language development predicts that vocalizations of 123 Exp Brain Res (2008) 184:599–603 infants aged between 8 and 13 months are aVected by the size of simultaneously manipulated objects. In other words, the results of the manual explorative activity, i.e. intrinsic properties related to interactions with objects, can aVect vocalization and used to identify an object. In addition, if these properties are object of communication signal, they can aVect also vocalizations, which accompany request arm gestures. Methods Nine typically developing infants (four females and Wve males) recruited from nursery schools in Parma participated in the experiment. The Ethics Committee of the Medical Faculty of the University of Parma approved the study. Data obtained by the Italian version of the short Infant form of MacArthur-Bates Communicative Development Inventory (CDI) questionnaire Wlled in by the infants’ parents (Caselli et al. 2006) are reported in Table 1. Data were used to establish the stage of children language acquisition: according to the number of produced words two infants were in preverbal phase, whereas seven infants were in emergent lexicon phase (Clark 2003). All infants were able to execute complex actions with objects. Request gestures were observed in all the infants, whereas declarative gestures (i.e. pointing gestures by which infants share attention and interest with adults to objects and events; Liszkowski et al. 2004) were observed in seven infants. The infants were tested at their homes. During the experimental session the infant sat on a child-chair in front of a table where the stimuli were presented; the experimenter and her/his mother sat behind the table in front of the infant. The stimuli were wooden objects (cube, cylinder, ball, cup and car) of two sizes: small object (side of 2 cm) and large object (side of 4 cm). The procedure was the following: the experimenter showed the object to the infant and manipulated it (mean duration 1.8 s, range 1–2 s). Only one object was presented at time, whereas the others were kept hidden in a box. Objects were presented in random sequence. The object attracted the attention of the infant, who was curious and urged to get in contact with that by executing a request arm gesture towards it. Then, the object was placed on the table plane at reachable distance, and the infant after reachinggrasping, manipulated it with his/her hand(s) (mean duration 3.6 s, range 1–7 s). Then, a new object was presented. A digital camcorder and a professional microphone were used to videotape the experimental session. They were placed at a Wxed distance of 2 m from the infant. The videotapes were transferred on a laptop and coded by two judges in separate sessions. The judges marked each vocalization produced by the infant while he/she manipulated or executed request arm gesture towards the object. Vocalizations were not grouped into categories. Agreement between Exp Brain Res (2008) 184:599–603 601 Table 1 Communicative and linguistic abilities of the infants tested in the present study Name Age (months) Comprehended words Produced words Produced actions and gestures Canonical babbling Post-canonical babbling Request gestures Declarative gestures 1 I.D. 12 22 1 7 Yes Yes Yes Yes 2 A.P. 13 20 2 11 Yes Yes Yes Yes 3 N.M. 12 37 5 12 Yes Yes Yes No 4 A.C. 12 18 8 7 Yes Yes Yes Yes 5 S.P. 13 12 0 4 Yes No Yes Yes 6 L.D. 12 49 2 10 Yes No Yes Yes 7 A.F. 12 33 0 12 Yes Yes Yes No 8 P.T. 11 35 5 7 Yes Yes Yes Yes 9 V.M. 13 45 11 10 Yes Yes Yes Yes coders was about 98% in classifying the vocalizations and 95% in classifying the gestures. Only trials selected by both the judges were included in the successive analyses. In summary, we analyzed one set of vocalizations during manipulation and one set during request arm gesture for each of the ten diVerent stimuli (Wve objects £ 2 dimensions). The total vocalizations were 747: the pronounced syllables were 75, which were not included in the analyses. Indeed, the syllables are incomparable with simple vocalizations, since formant transition modiWes mean formant values. The total number of vocalizations during the two manual activities was 261: 31% were discarded because they were emitted during request arm gestures directed to unidentiWed objects inside the box. The mean number of vocalization per infant selected in order to be included in the successive analyses was 20, median: 18, range: 14–26 (vocalization number in the large object condition, mean 9.3, median 8, range 7–14; vocalization number in the small object condition, mean 10.7, median 9, range 7–17). From the audio track, we analyzed the voice spectrograms of the vocalizations using the Praat software (www.praat.org). We computed the following voice parameters: Intensity, Pitch, F1 and F2. It is well known that voice formants are the frequencies that exactly deWne a vowel from an acoustical point of view (Leoni and Maturi 2002) and can be distinguished already in spectrograms recorded during spontaneous infants’ vocalizations (Gilbert et al. 1997). We calculated the Standard Deviation (SD) of each parameter. The voice parameters and their SDs during manipulation and request gesture were submitted to Analyses of Variance (ANOVAs) whose within subjects factors were object size (small vs. large) and activity (manipulation vs request arm gesture). Results Figure 1 shows typical examples of manipulation (Fig. 1a) and of request arm gesture (Fig. 1b) of an infant who vocal- ized during the two activities. The infants manipulated the objects using one (51% out of the manipulations) or two hands (49% out of the manipulations). About 53% out of the manipulations of the small object were executed with two hands (47% with one hand), and 46% out of the manipulations of the large object were executed with two hands (54% with one hand). In other words, the infants used more frequently two hands to manipulate small than large objects. This indicates that the eVects on vocalization (see below) were not due to commands to one and two hands when manipulating small and large objects, respectively. Mouthing, Wngering, shifting the object from hand to hand, rotating, activities typical of infants aged between the 6– 12 months were also observed. However, vocalizations during these activities were not found. The infants performed request arm gestures by extending only one arm towards the object in most (91%) of the cases. All Wngers or only the index Wnger (while the others were Xexed) were extended. In both the two activities the infant while vocalizing directed always her/his gaze towards the object. However, the infants looked at the experimenter or at the mother before or after vocalization in 26% out of the manipulation activities, and in 17% out of the request arm gesture activities. In the remaining cases they Wxated the object till the experimenter gave it to them. Since the distribution of the F1 values was skewed (1.07) we performed a logarithmic transformation on the data, which reduced the skeweness to 0.4. The skewness of the other analyzed parameters was less than 0.32. Figure 1 shows the main results of the statistical analyses performed on voice spectra parameters. The size of the object aVected F1 (Fig. 1c) during manipulation and gesturing (F(1,8) = 11.4, P < 0.01, 2 = 0.135, f = 0.39). F1 was higher when the activity was directed to large than to small objects (mean 797 vs. 750 Hz, median 766 vs. 724 Hz, range 458–1288 vs. 479–1244 Hz). In addition, F1 (F(1,8) = 4.7, P = 0.06, 2 = 0.095, f = 0.32 Fig. 1c) and SD of F1 (F(1,8) = 5.2, P = 0.053, 2 = 0.036, f = 0.19, 123 602 Exp Brain Res (2008) 184:599–603 Fig. 1 Upper panels: examples of manipulation (a) and request arm gesture (b) of an infant tested in the present study, who vocalized during the manual activities. The object guiding the motor activity was a large solid. Lower panels: variation in F1 (c) and Standard Deviations (SD) of F1 (d) as a function of object size when the infants vocalized during manipulation of and request arm gesture towards small and large objects. Note that logarithms of F1 are reported in c. Error bars are standard errors Fig. 1d) showed a trend to increase in request arm gesture than in manipulation. The eVect on SD of F1 was signiWcant for the large object (interaction between size and activity, F(1,8) = 5.8, P < 0.05, 2 = 0.102, f = 0.34, Fig. 1d). Finally, SD of the voice intensity was higher in request arm gesture than in manipulation (F(1,8) = 9.1, P = 0.01, 2 = 0.096, f = 0.32, 5.7 vs. 3.9 db). No signiWcance was found in the ANOVAs performed on the other voice parameters. Discussion The vocalizations of the infants were modulated by the size of the object during the activities of manipulation and gesturing. SpeciWcally, F1 was higher when the object was large than when it was small. This eVect might be interpreted as consequent only to the visual analysis of the object since the infant Wxated the stimulus during the vocalizations. In other words, it could depend on arousal (i.e., larger objects are more interesting and therefore more arousing for infants). However, if this were true, we should Wnd an eVect on all the voice parameters and especially on voice intensity. This was not observed. In addition, the results concerning SD of F1 indicate that voice modulation as a function of object size was less variable during manipulation than during gesture. This suggests a stricter relation between hand and mouth when the hand directly interacted with the object. To explain this relation, we propose that intrinsic object properties elic- 123 ited manipulation commands, which were sent to the hands as well as to the mouth (Gentilucci et al. 2001). Moreover, F1 is related to internal mouth aperture: that is, higher F1 is associated to larger mouth aperture (Leoni and Maturi 2002). Consequently, the command to open the Wngers by a larger amount (i.e. during manipulation of the large object) was sent also to the mouth whose aperture was further enlarged producing higher vocalization. Moreover, we hypothesize that when an object held in the experimenter’s hand was visually presented to the infants, manipulation commands to both the hand and the mouth were activated by a mirror system. They induced the same eVects on the voice of infants gesturing to the object as they did on the voice of infants manipulating the same object. However, the commands were not precise because the object was not held in the infants’ hands and no somaesthesic information on object size and/or no vision of their manipulating hand(s) were provided. Thus, variability of mouth aperture and voice increased (see results concerning SD of F1). A problem concerning the data of the present study is whether the infants’ arm movements directed towards the objects were request gestures. According to Butcher and Goldin-Meadow (2000), request gesture is deWned as the infant’s arm movement during which he points to the object and alternatively directs the gaze to the object and to the adult who is able to satisfy his implicit request of possession. In the present experiment, the gaze was only occasionally directed to the experimenter or to the mother. However, the Exp Brain Res (2008) 184:599–603 fact that the infant vocalized indicates that he/she attracted the attention of the adult on the object pointed to and speciWed by voice parameters. In other words, from a functional point of view vocalization might substitute gaze. In accordance with this hypothesis, Pizzuto and colleagues (Pizzuto et al. 2005, see also Iverson et al. 1994) proposed that the vocalization reinforces deictic gesture making the request of attention more salient than when it is conveyed by gaze. The fact that manipulation commands can be associated to request gestures towards an object can be explained by the proposal of Vygotskij (1934) that request gestures derive from reaching to grasp movements, i.e. from actions guided by object intrinsic properties like the manipulation activity is (Lock 1978). The process of transformation from reaching-grasping to request gesture can be brieXy explained as follows: usually, when the infant fails to reach and grasp an object, the adult automatically grasps and oVer it to the infant. This, in turn, induces the infant to execute the reaching-to-grasp gesture even towards unreachable objects in the expectancy to receive them from the adult. Through time, these gestures lose the feature of transitive action and acquire a communicative intent. The results of the present experiment are in agreement with data of previous studies carried out on adults in which the observation/execution of transitive actions (i.e. guided by an object) aVected the voice of syllables pronounced simultaneously with action execution (Gentilucci 2003; Gentilucci et al. 2001; Gentilucci 2004a,b). Interestingly, the observation of action pantomimes aVected the voicing of syllables as the transitive action did (Gentilucci et al. 2004a). This suggested that the type of interaction of the hand with the object, rather than the object per se, could inXuence speech. Consequently, even if this is not testable in infants, commands of manual interactions (i.e. the motor representations of manual interactions) might be used as a primitive form of object identiWcation. Once transformed in vocalization they might be used to communicate with other individuals (request arm gesture activity). Acknowledgements We wish to thank the personnel of the nursery schools (Educational Services of Comune di Parma) for their help in contacting the families. We especially thank the infants who participated in the study and their parents. We are very grateful to Virginia Volterra for discussion of the data and comments on an early version of the paper. We thank Aaron Shield for the comments on the manuscript. The work was supported by MIUR (Ministero dell’Istruzione, dell’Università e della Ricerca) and by Fondazione Monte Parma. References Bates E (1976) Language and context. The acquisition of pragmatics. Academic, New York Bates E, Dick F (2002) Language, gesture, and the developing brain. Dev Psychobiol 40(3):293–310 603 Bernardis P, Gentilucci M (2006) Speech and gesture share the same communication system. Neuropsychologia 44:178–190 Butcher C, Goldin-Meadow S (2000) Gesture and the transition from one- to two-word speech: when hand and mouth come together. 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