Developmental Psychobiology

Miche`le Molina1 Coralie Sann1 Morgane David1 Yacine Toure´2 Bernard Guillois2 Franc¸ois Jouen3 1

2

Psychologie des Actions Langagie`res et Motrices Universite´ de Caen-Basse Normandie Esplanade de la Paix EA4649 Caen F-14032, France E-mail: [email protected]

Centre Hospitalier Universitaire-Service de Ne´onatalogie Avenue de la Coˆte de Nacre Caen, F-14033 France 3

Cognitions Humaine et Artificielle Ecole Pratique des Hautes Etudes 4–14 rue Ferrus EA 4004 Paris F-75014, France

Active Touch in Late-Preterm and Early-Term Neonates ABSTRACT: An infant-controlled tactile habituation without visual control procedure was used to evaluate the ability of 32 late-preterm neonates (mean gestational age: 34 weeks) and 32 early-term neonates (mean gestational age: 38 weeks) to actively explore with hands objects varying in texture (smooth, granular). Holding time and Hand Pressure Frequency (HPF) were recorded. Holding time decreased as habituation progressed in both group of neonates. Holding time increased from habituation trials to test trials only in early-term neonates. A reaction to novelty was only observed in early-term neonates. During habituation, HPF remained unchanged in late-preterm infants whereas HPF decreased in early-term infants. HPF increased from habituation trials to test trials in early-term neonates and in late-preterm infants. However, reaction to novelty was only observed for early-term infants. The significance of these results is discussed in reference to brain maturation in preterm infants. ß 2015 Wiley Periodicals, Inc. Dev Psychobiol 57:322–335, 2015. Keywords: late-preterm neonates; early-term neonates; active touch; haptic exploration; grasping; modulation

INTRODUCTION The World Health Organization defines preterm birth as a birth occurring before 37 completed weeks of gestation. The normal term of birth varies from 37 to 41 weeks of gestation (about 280 days) since the first day of the mother’s last menstrual period. Preterm neonates, born before 37 weeks of gestation, differ from full-term neonates according to the degree of brain maturation, which is related to the gestational age (GA) in weeks at birth (Mento & Bisiachi, 2012). A fundamental issue concerns the capacity of preterm infant to actively interact with environment in spite of the neurological immaturity. Studies conducted on tactile perception help to shed light on this question. Classically two kinds of haptic perception are identified: active touch and passive touch (Gibson, 1962). Active touch is a self-generated exploration that occurs when people use fingers and hand movements in order to explore properties of an object. In contrast, passive Manuscript Received: 24 March 2014 Manuscript Accepted: 20 January 2015 Correspondence to: Miche`le Molina Article first published online in Wiley Online Library (wileyonlinelibrary.com).18 March 2015 DOI 10.1002/dev.21295  ß 2015 Wiley Periodicals, Inc.

touch does not involve movement of the hands and fingers: The stimulus is simply impressed on skin. Receptors and neural pathways associated with haptic perception are long known to be the first to develop in utero (Kandel, Schwartz, & Jessell, 2000), allowing fetuses and preterm infants to react to passive tactile stimulations applied on various part of their body. Observations of aborted fetuses have revealed that responses to tactile stimulations are observed since the 7th week of gestation (Hooker, 1938; Humphrey, 1964, 1970). Recent neuroimaging studies (Roche-Labarbe, Wallois, Ponchel, Kongolo & Grebe, 2007) report somatosensory cortical responses to passive tactile stimulation of the hand in preterm infants aged of 33– 34 weeks of gestational age and confirm earlier findings stated by behavioral researches. For instance, Fearon, Hains, Muir and Kisilevski (2002) have demonstrated that 30 weeks GA preterm infants were able to get habituated and to discriminate passive tactile stimulations delivered on the arm. Countless studies have reported that preterm infants benefit from passive touch stimulations and massage therapy (for a review see Field, Diego, & Hernandez-Reif, 2010). More recently, (Lejeune et al., 2010) demonstrated that preterm infants, ranging from 33 to 34 þ 6 weeks post-conceptional age (PCA) with a mean post-natal age of 474 hr,

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Developmental Psychobiology

are also able of active touch for different shapes of objects (e.g., prism vs. cylinder). Using a habituation paradigm, these authors observed that following a habituation period with an object, neonates held longer a new shaped object compared to the object they were habituated to. These results were replicated in very preterm infants assessed before the PCA of 32 weeks (Marcus, Lejeune, Berne-Aude´oud, Gentaz & Debillon, 2012). Lejeune et al. (2012) have also demonstrated that preterm infants are able to transfer shape information from one hand to the other: After habituation to the shape of an object in one hand, preterm infants held the novel object longer in the other hand. In a recent study Lejeune, Berne-Aude´oud, Marcus, Debillon, and Gentaz (2014) confirmed that tactile manual habituation and discrimination of shape information is observed in preterm infants at a post-conceptional age of 34 weeks, independently of postnatal age. These elegant studies exclusively based on the recording of holding time converge to a major conclusion: Around 33 weeks of PCA, the grasping of preterm neonates would not be only a reflex activity because preterm infants are able of haptic habituation and discrimination of shape with the hand. Preterm infants could use grasping behavior as an exploratory tool to get some specific information about the shape of the object. However these studies raise an important question concerning the way preterm neonates haptically process object properties. As a matter of fact, holding time is a decent descriptor of attention orientation toward the objects presented during habituation and test sequences but does not give any indication about the characteristics of the haptic exploratory behavior ineludibly developed to pick up information about object properties. As underlined by Lederman and Klatzky (1987); any purposive hand movements leading to active perception of object property necessarily result in various and successive contact between hand and object. Studies based on the recording of hand pressure exerted on held objects (Rochat, 1987; Molina & Jouen, 1998) have clearly revealed full-term neonates’ skills to actively explore an object with their hands. These studies have revealed that in full-term neonates, the palmar grasping activity is object-dependent rather than under control of reflexive mechanisms triggered by any kind of stimulation (Jouen & Molina, 2005). For instance, Molina and Jouen (1998, 2003) observed that full-term neonates modulate grasping activity according to the texture of objects: Higher hand pressure frequency (HPF) was recorded when neonates grasped smooth objects in comparison to granular objects. Moreover, applying HPF analysis to haptic habituation, Molina and Jouen (2004) also demonstrated that neonate’s manual activity is a dynamic

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process that takes place over time and allows discovering properties about objects: HPF activity decreased over successive presentation of a same object in the infant’s hand, revealing a habituation phenomenon of exploratory behavior in neonates. The present research is devoted to study if this kind of dynamic haptic process demonstrated in full-term neonates can also be observed in preterm. More specifically, the main purpose was to investigate when this kind of dynamic haptic process appears during development according to brain maturity. To reach this point, we constituted two groups of neonates varying only according to gestational age in weeks (GW) but matched for experiential age: 34 GW and 38 GW. Thirty-eight gestational age in weeks was selected as upper limit for the study since Jouen, Sann and Molina (2012) have demonstrated that dynamic haptic process is observed in 39–40 GW full-term infants. Thirty-eight GW are the youngest neonates among the full-term population and can be considered as control group. The lower 34 GW age was chosen according to studies that have demonstrated that cortical integration of haptic information can be observed around this gestational age (Nevalainen, Lauronen, & Pihko, 2014). According to The American College of Obstetricians and Gynecologists and the Society for Maternal-Fetal Medicine, 34 GW infants are considered as late-preterm and 38 GW neonates as early-term. We performed a classic tactile habituation/reaction to novelty procedure without visual control. In addition to holding time variable, we measured and analyzed hand pressure frequency during habituation and test periods. Concerning holding time variable, we expect a significant decrease during habituation and a significant increase of the holding time for the presentation of the novel texture during the test phase. Concerning hand pressure frequency variable, if neonates actively explore texture, a significant decrease of frequency should be observed during habituation as well as a modulation according to the texture of objects. During the test phase, we expect an increase of frequency for the presentation of the novel texture. Based on the previous quoted studies, these effects are expected in both groups of neonates.

METHOD Participants The present study was conducted in accordance with the declaration of Helsinki and approved by the French North West Ethic Committee (CPP n˚2010-A00120– 39). All participants were observed after the parents

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gave written consent to participate in the experiment. Haptic exploration of texture property was studied in preterm neonates born before 37 GA weeks and in early term neonates born between 37 and 38 weeks of gestation. Thirty-eight late-preterm neonates (19 girls and 19 boys) were recruited in intensive and regular neonatal care units of the University Hospital Center of Caen. Six were rejected because of fussing (N ¼ 1) and sleeping (N ¼ 5) during data recording. Final sampling consisted of thirty-two late-preterm neonates (17 girls and 15 boys). Thirty-nine early-term neonates (13 girls and 26 boys) were enlisted from the maternity unit of the University Hospital Center of Caen. Seven were rejected because of fussing (N ¼ 2), sleeping (N ¼ 4), and experimenter’s error (N ¼ 1) during data recording. Final sampling consisted of thirty-two early-term neonates (10 girls and 22 boys). To be included in the study, all infants had to exhibit spontaneous breathing, grasping reflex, to be not affected by any polymalformative syndrome, to be awake, and to have received neither sedative nor anticonvulsive treatment during 24 hr preceding the study. Were excluded from the study hypotrophic neonates. Transfontanellar echography was used in latepreterm neonates to exclude those presenting intraventricular hemorrhage and periventricular leukomalacia. As shown in Table 1, late-preterm and early-term neonates differed according to their gestational age, weight at birth, and cranial perimeter. Although neonates were observed within the third and the sixth day after birth, they nevertheless differed according to their chronological age with early-term neonates being observed around the fourth day and late-preterm neonates around the fifth day of life.

and maintained by a nylon wire. Pearls were attached in a pseudo-random configuration. By definition, the texture density ratio of the smooth object was equal to 0 and the texture density ratio of the granular object was equal to .05 (total surface covered by the pearls/ total surface of the object). Cylindrical objects were adapted to the size of the neonate’s hand (Fig. 1). Objects presented to early-term neonates were 55 mm cm in length and 10 mm in diameter. Objects presented to late-preterm neonates were 55 mm in length and 5 mm in diameter. Objects were connected to a piezo resistive pressure sensor (ALCATEL Model DS1), which allowed recording of a differential positive pressure for up to 1.7 MPa. Prior to any experiment, we verified that the presence of pearls did not affect the rigidity of the object. For an equal pressure exerted on each object, a signal of the same magnitude was obtained. Pressure sensor was also tuned to be not affected by the size of used objects for each group of neonates. Right hand pressure exerted on the object was continuously sampled by a 16-bit A/D converter at a rate of 36 Hz and stored on a PC compatible computer for further analysis. In order to limit the aliasing effects of high frequency components, the signal was submitted to a filter involving FFT smoothing over a six measures mobile window and eliminating all frequencies equal to or above 4 Hz. The smoothing was accomplished by removing Fourier components with frequencies higher than 1/(n*Dt) where n is the number of data points considered at a time (5), and Dt is the time spacing between two adjacent data points (.027 s). Constant component and linear trend of the sample signal were also removed numerically. Each acquisition file contained N samples (36 Hz  duration in s), which therefore corresponds to the time series of the hand pressure.

Stimuli Natural latex droppers were used to design the objects used in this experiment. Objects varied only according to their texture density. The smooth object consisted of the uniform rubber surface without any texture. The granular object consisted of the same rubber surface on which 2 mm thin plastic pearls were added

Procedure Before testing, each infant’s arousal was stimulated according to Grenier’s method Grenier, (1981) to ensure that the newborn was in a state of alert inactivity at the beginning of the experiment. Behavioral state was also evaluated for each successive trial: Late-

Table 1. Characteristics (Mean, SD and Range) of Late-Preterm and Early-Term Infants Late-Preterm Neonates

Gestational age in weeks Weight at birth in g Cranial circumference in cm Chronological age in days

Early-Term Neonates

Statistics

M

SD

Range

M

SD

Range

t(1–62)

p

34.5 2227.09 31. 75 5

.72 362.10 1.44 1.08

33–35.4 1440–2940 29–32.91 3–6

38.2 3106.45 34.54 4

.58 408.7 1.9 .92

37–38.6 2260–3920 33–35.4 3–6

21.66 9.04 7.96 2.60

0.0001 0.0001 0.0001 0.01

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test period began. Each baby received two test trials, with each trial following the same procedure as the habituation trials.

Data Processing

FIGURE 1 Smooth and granular objects.

preterm and early-term newborns were tested in state four according to the NBAS. All the infants were observed in the morning after bathing and about 1 hr after the last feeding. All participants were placed in the mother’s arm, in a semi-reclined position, facing the experimenter. They were free to move their arms. Moreover, the tested-hand (the right one) of neonates was free of any perfusion or scope monitoring. Infant-controlled haptic habituation without visual control procedure was used. In each group of neonates (late-preterm and early-term), half of the 32 infants received haptic habituation with a smooth object and the other half with a granular object. Infants were then randomly assigned to a test condition involving either a novel object or a familiar object. The habituation period began as Experimenter 1 introduced an object in the right hand of the infant by holding the object at its junction with the air pressure tubing. As soon as the infant grasped the object, the first experimenter signaled the beginning of a trial to a second experimenter and prevented the infant to look at the object by placing his/her hand between the held object and the infant’s gaze. A trial ended when the baby released the object or after 60 s of continuous holding. In this latter case, Experimenter 1 gently opened the baby’s hand and removed the object. Data sampling was programmed to stop whenever the baby held the object for less than one second. Trials were continued until nine trials had occurred or until a criterion of habituation had been met, whichever came first. The criterion for habituation was the same as that used by Streri, Lhote and Dutilleul (2000). The infant was judged to have been habituated when the duration of holding on any two consecutive trials, from the third trial onwards, totaled a third or less of the total of the first two trials. Therefore, each infant received between four and nine habituation trials. After the last habituation trial, the

In order to quantify the habituation phenomena for texture, holding time (in seconds) and hand pressure frequency (in Hertz) were computed throughout the habituation. Due to the use of an infant controlled procedure, spectral analyses such as the Fast Fourier Transform could not be directly applied to analyze hand pressure frequency. As such, individual time series of positive hand pressure (expressed in volts) were analyzed using the technique of peak analysis initially developed by Molina and Jouen (1998). Since the technique was described in greater detail in previous studies, only general principles of peak picking will be explained here. Prior to any calculation, the mean pressure and standard deviation were calculated from the original signal for each time series of the sampled hand pressure. The method for peak picking uses a moving window over successive hand pressures. The height of the moving window was equal to 1 SD and its width was equal to five points. To be recognized as a peak, sampled values must be found outside this mobile window in the Y range. Only pressures over 1 SD were identified as a peak if the duration of the response was equal to or above 250 ms in the X range. This allowed the calculation of the number of peaks. From these data, the reduction peak frequency was derived. The hand pressure frequency (HPF, expressed in Hz) is the ratio of the peak number divided by the period duration (holding time).

RESULTS Preliminary Data Analyses Since recent studies have recently suggested an early female advantage in fine motor behavior (see Alexander & Wilcox, 2012 for details), a first series of analyses was conducted in order to evaluate the existence of any differences between the male and the female participants for holding time and hand pressure frequency. Table 2 summarizes total holding times, holding times for the first two trials, holding times for the last two trials and numbers of trials to reach habituation criterion for females and males in each group of neonates (early-term vs. late-preterm). In order to evaluate whether group or sex affected the habituation measures, a 2 Groups (early-term vs. late-preterm)  Sex (female vs. male) ANOVA was performed for each indicator.

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Table 2. Total Holding Times (in Seconds), Holding Times for the First Two Trials (in Seconds), the Last Two Trials (in Seconds), and Mean Numbers of Trials During Habituation According to Groups (Early-Term vs. Late-Preterm) and Sex. SDs are Given Into Brackets

Groups Early-Term (N ¼ 32) Late-Preterm (N ¼ 32)

Sex Girls Boys Girls Boys

(10) (22) (13) (19)

Holding Time (s) Throughout the Habituation Period 59,66 72,19 96,22 89,33

(60.28) (35.08) (54.28) (44.88)

Concerning the total holding time, a significant effect of group was observed, F(1, 60) ¼ 4.83, p ¼ .031, a ¼ .58, revealing that late-preterm neonates held the object for longer amount of time (M ¼ 92.13 s, SD ¼ 48.18) than early-term neonates (M ¼ 68.27 s, SD ¼ 43.86). No significant effect of sex, F(1, 60) ¼ .053, p ¼ .818, a ¼ .055 nor interaction between sex and group, F (1, 60) ¼ .63, p ¼ 0.43, a ¼ .122 were observed suggesting that holding time all over the habituation period did not vary according to the neonate’s sex. A significant effect of group, F(1, 60) ¼ 7.296, p ¼ .008, a ¼ .757 was noticed for the holding time of the first two trials, revealing that late-preterm neonates held longer the objects (M ¼ 46.06 s, SD ¼ 41.78) than early-term neonates (M ¼ 21.77 s, SD ¼ 28.22). No significant effect of sex, F(1, 60) ¼ .35, p ¼ .55, a ¼ .09 nor interaction between sex and group, F(1, 60) ¼ .08, p ¼ .77, a ¼ .059 were observed suggesting that holding time during the two first trials did not vary according to the neonate’s sex. Significant effect of group, F(1, 60) ¼ 5.79, p ¼ .019, a ¼ .66, was also noticed for the holding time of the last two trials, revealing that late-preterm neonates held the object longer (M ¼ 16.56 s, SD ¼ 14.77) than early-term neonates (M ¼ 9.68 s, SD ¼ 7.86). No significant effect of sex, F(1, 60) ¼ .18, p ¼ .667, a ¼ .07 nor interaction between sex and group, F(1, 60) ¼ .40, p ¼ .53, a ¼ .09 were observed suggesting that holding time all over the habituation period did not vary according to the neonate’s sex. ANOVA revealed a significant effect of group, F(1, 60) ¼ 9.09, p ¼ .003, a ¼ .84, revealing that early-term neonates needed more trials to get habituated (M ¼ 7.62 , SD ¼ 1.43) than late-preterm neonates (M ¼ 6.03, SD ¼ 1.97). No significant effect of sex, F (1, 60) ¼ .03, p ¼ .95, a ¼ .05 nor interaction between sex and group, F(1, 60) ¼ 3.92, p ¼ .053, a ¼ .49 were observed suggesting that the number of trials to reach habituation did not vary according to the neonate’s sex.

Holding Time (s) During the First Two Trials 16.04 24.37 44.32 47.26

(23.99) (30.11) (42.91) (42.14)

Holding Time (s) During the Last Two Trials

Number of Trials (N) to Reach Criterion of Habituation

7.38 (5.72) 10.73 (8.58) 16.94 (11.56) 16.30 (16.93)

7 (1.85) 7.9 (1.15) 6.53 (2.06) 5.68 (1.89)

Similar analyses were performed on hand pressure frequency (Table 3). ANOVA failed to reveal a significant effect of group, F(1, 60) ¼ 3.3, p ¼ .074, a ¼ .43, for the amount of HPF recorded all over the habituation period. No significant effect of sex, F(1, 60) ¼ .305, p ¼ .58, a ¼ .08 nor interaction between sex and group, F(1, 60) ¼ .001, p ¼ .97, a ¼ .05 were observed. Concerning the HPF recorded during the two first trials, ANOVA revealed a significant effect of group, F (1, 60) ¼ 4.94, p ¼ .029, a ¼ .59, such that early-term neonates exhibited higher HPF (M ¼ .63 Hz, SD ¼ .69) than late-preterm neonates (M ¼ .32 Hz, SD ¼ .27). No significant effect of sex, F(1, 60) ¼ .31, p ¼ .58, a ¼ .08 nor interaction between sex and group, F(1, 60) ¼ .398, p ¼ .53, a ¼ .09 were observed suggesting that HPF did not vary according to the neonate’s sex. HPF recorded during the two last trials did not significantly differ across groups, F(1, 60) ¼ 1.156, p ¼ .286, a ¼ .18. No significant effect of sex, F(1, 60) ¼ .058, p ¼ .809, a ¼ .056 nor interaction between sex and group, F(1, 60) ¼ .70, p ¼ .40, a ¼ .13, were noticed suggesting that HPF during the two last trails did not vary according to the neonate’s sex. Since no significant effect of sex was observed for hodling time and HPF, sex of participants was not included as an additional variable in the next performed ANOVAs.

Holding Time Habituation Period. All the late-preterm neonates and early-term neonates reached the criterion of habituation (Table 4). Infants’ holding time (in seconds) during habituation trials was analyzed with a 2  2  4 mixedmodel ANOVA with Group (early-term vs. late-preterm), Habituation object (smooth vs. granular) as a between subjects factors and with Trials (first, second, second last, and last trials of habituation) as a within subjects factor. The main effect of Habituation object

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Table 3. Total Hand Pressure Frequency (in Hz), Hand Pressure Frequency (in Hz) During the First Two Trials, and During the Last Two Trials (in Hz) According to Groups (Early-Term vs. Late-Preterm) and Sex. SDs are Given Into Brackets

Groups Early-Term (N ¼ 32) Late-Preterm (N ¼ 32)

Sex Girls Boys Girls Boys

HPF (Hz) Throughout the Habituation Period

(N ¼ 10) (N ¼ 22) (N ¼ 13) (N ¼ 19)

1.6 (1.35) 1.88 (2.78) .77 (.39) 1.01 (.73)

was not significant, F(1, 60) ¼ .08, p ¼ .78, a ¼ .06. This suggests that for both groups of infants, habituation rate did not differ in reference to the texture of objects, as also suggested by a non-significant group x habituation object interaction, F(1,60) ¼ .001, p ¼ .97, a ¼ .05. For both objects, a main effect of the trials was observed, F(3, 180) ¼ 12.08, p < .00001, a ¼ .99, enlightening that in each group, holding times decreased as habituation progressed. ANOVA also revealed a significant effect of the Group factor, F(1, 60) ¼ 9.60, p ¼ .003, a ¼ .86, revealing that during the trials of habituation, late-preterm infants hold the objects for longer duration (M ¼ 92.13 s, SD ¼ 48.65) than early-term infants (M ¼ 68.27 s, SD ¼ 41.79). No other significant effects were observed. Table 4 summarizes total holding times, holding times for the first two trials, for the last two trials, and numbers of trials to reach habituation criterion for both groups of infants and for both objects. In order to evaluate whether group or texture affected the habituation measures, a 2 Groups (early-term vs. latepreterm)  2 Habituation objects (smooth vs. granular) ANOVA was performed for each indicator. Concerning the mean total holding time, no significant effect of the Habituation object, F(1, 60) ¼ .13, p ¼ .72, a ¼ .064 was observed. A significant effect of the Group factor was observed, F(1, 60) ¼ 4.24, p ¼ .043, a ¼ .525, revealing that late-preterm infants (M ¼ 92.13 s, SD

HPF (Hz) During the First Two Trials .64 .63 .24 .41

(.67) (.71) (.25) (.30)

HPF (Hz) During the Last Two Trials .25 .17 .27 .32

(.36) (.20) (.24) (.41)

¼ 48.65) held objects longer than early-term neonates (M ¼ 68.27 s, SD ¼ 41.79). No significant effect of the Habituation object, F(1, 60) ¼ .05, p ¼ .82, a ¼ .06 was noticed for the mean holding time of the first two trials. There was a significant effect of the Group factor, F(1, 60) ¼ 7.20, p ¼ .009, a ¼ .751, such as latepreterm infants (M ¼ 46.06 s, SD ¼ 41.8) held objects for longer period than early-term infants (M ¼ 21.76 s, SD ¼ 28.2). No significant effect of the habituation object, F(1, 60) ¼ .065, p ¼ .025, a ¼ 0.61 was noticed for the mean of the two last trials of habituation. There was only a significant effect of the Group Factor, F(1, 60) ¼ 5.23, p ¼ .025, a ¼ .61, such as late-preterm infant (M ¼ 16.56 s, SD ¼ 14.77) held objects for longer period than early—term infants (M ¼ 9.68 s, SD ¼ 7.86). Finally, for the mean number of trials required to reach habituation, no significant effect of the Habituation object, F(1, 60) ¼ .42, p ¼ .52, a ¼ .09 was present, and a significant effect of the Group factor was observed, F(1, 60) ¼ 13.34, p < .001, a ¼ .95, demonstrating that early-term infants (M ¼ 7.63, SD ¼ 1.43) needed more trials to reach the criterion of habituation than late-preterm infants (M ¼ 6.03, SD ¼ 1.97). Taken together, these analyses revealed that in each group of neonates, tactile habituation occurred for both smooth and granular objects (Fig. 2). However, these analyses also demonstrated that habituation rate dif-

Table 4. Total Holding Times (in Seconds), Holding Times for the First Two Trials (in Seconds), the Last Two Trials in Seconds), and Mean Numbers of Trials During Habituation According to Infants (Early-Term vs. Late-Preterm) and Objects (Smooth vs. Granular). SDs are Given Into Brackets.

Groups Early-Term (N ¼ 32) Late-Preterm (N ¼ 32)

Habituation Object

Holding Time (s) Throughout the Habituation Period

Smooth (N ¼ 16) Granular (N ¼ 16) Smooth (N ¼ 16) Granular (N ¼ 16)

60.18 (28.71) 76.36 (54.88) 96.09 (52.6) 88.17 (44.70)

Holding Time (s) During the First Two Trials 21.78 21.76 48.10 44.02

(31.29) (25.82) (43.66) (41.14)

Holding Time (s) During the Last Two Trials 10.43 (6.21) 8.94 (6.19) 16.58 (17.67) 16.54 (11.78)

Number of Trials to Reach Criterion of Habituation 7.69 7.56 6.25 5.81

(1.45) (1.46) (1.98) (2.01)

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FIGURE 2 Holding time in s (mean and standard error) for granular (left part of the graph) and smooth (right part of the graph) objects during the 4 trials of the habituation period and the 2 test trials for late-preterm (upper part of graph) and early-term infants (lower part of graph).

fered across groups with late-preterm neonates requiring less but longer trials to get habituated than earlyterm infants.

Test Period Holding times (in seconds) during test trials were analyzed with a 2  2  2  2 mixed-model ANOVA with Group (early-term vs. late-preterm), Habituation object (smooth vs. granular) and Test object (new vs. familiar) as between subjects factors and with Trials (first and second test trials) as a within Subject factor. ANOVA failed to reveal any significant effect of the Group factor, F(1, 56) ¼ 2.39, p ¼ .53, a ¼ .33, the Habituation object, F(1, 56) ¼ .39, p ¼ .53, a ¼ .09, the Test object, F(1, 56) ¼ 1.23, p ¼ .27, a ¼ .19 and the Trials, F(1, 56) ¼ .89, p ¼ .35, a ¼ .15. ANOVA revealed a significant Habituation object  Test object interaction, F(1, 56) ¼ 10.32, p ¼ .002, a ¼ .88 (Fig. 2). Planned comparisons were performed to assess this interaction. After habituation to the smooth object, although holding times were longer for the new

granular object (M ¼ 22.68 s, SD ¼ 20.03) than for the familiar smooth object (M ¼ 7.20 s, SD ¼ 9.75), the difference was not statistically significant, F(1, 56) ¼ .41, p ¼ .66. Similarly, after habituation to the granular object, although holding times were longer for the new smooth object (M ¼ 16.46 s, SD ¼ 15.74) than for the familiar granular object (M ¼ 8.93 s, SD ¼ 8.77), F(1, 56) ¼ 1.19, p ¼ .31, the difference did not reach significant level. This puzzling result could be related to a significant Habituation object  Group factor  Trials interaction, F(1, 56) ¼ 4.17, p < .05, a ¼ .52. Fisher post hoc tests were thus performed to analyze this third order interaction. For early-term neonates, after habituation to a granular object, holding times did not vary from the first (M ¼ 11.18 s, SD ¼ 13.08) to the second test trial (M ¼ 11.52 s, SD ¼ 16.08), p ¼ .95. In the same way, after habituation to a smooth object, holding times did not also vary from the first (M ¼ 10.52 s, SD ¼ 17.72) to the second test trial (M ¼ 10.96 s, SD ¼ 19.39), p ¼ .93. For the late-preterm neonates, after habituation to the granular object, holding times did not vary from the first (M ¼ 17.02 s,

Developmental Psychobiology

SD ¼ 20.03) to the second test trial (M ¼ 11.03 s, SD ¼ 16.43), p ¼ .24. On the contrary, holding times following habituation with the smooth object varied from the first (M ¼ 11.75 s, SD ¼ 15.17) to the second test trial (M ¼ 26.52 s, SD ¼ 25.15), p ¼ .005. This post-hoc analysis underlined that contrary to what was observed in early-term neonates, holding times fluctuated from the first to the second test trial in late-preterm infants (Fig. 2). This unusual pattern of response might have prevented the observation of a significant reaction to novelty when both groups were pooled together for analysis. In consequence, holding times of preterm and early term neonates during test period were then separately analyzed.

Holding Time Analysis During Test Period in Late-Preterm Neonates Test trials were analyzed with a 2  2  2 mixed-model ANOVA with Habituation object (smooth vs. granular) and Test object (new vs. familiar) as between subjects factors and with Trials (first and second test trials) as a within subjects factor. The ANOVA failed to reveal any significant effect of the Habituation object, F(1, 28) ¼ .80, p ¼ .38, a ¼ .14, the Test object, F(1, 28) ¼ .64, p ¼ .43, a ¼ .12 nor the Trials, F(1, 28) ¼ 1.47, p ¼ .24, a ¼ .22. After habituation to the smooth object, late-preterm neonates tend to hold the new granular test object for longer periods (M ¼ 26.6 s, SD ¼ 20.39) compared to late-preterm neonates presented with the familiar smooth test object (M ¼ 11.65 s, SD ¼ 11.46). Similarly, after habituation to the granular object, late-preterm neonates tend to hold longer the new smooth object (M ¼ 16.86 s, SD ¼ 20.41) than late-preterm neonates presented with the familiar granular object (M ¼ 11.13 s, SD ¼ 8.89). Nevertheless, the Habituation object  Test object interaction was not significant, F(1, 28) ¼ 3.28, p ¼ .08, a ¼ .41. These differences failed to reach significance level due to an instability of holding times of the participants during the two test trials as revealed by a significant Habituation object  Trials interaction, F(1, 28) ¼ 8.20, p ¼ .008, a ¼ .79. Post hoc comparisons confirmed that following habituation with a granular object, whatever the held object during test trial (new or familiar), late-preterm neonates did not hold longer (p ¼ .25) test objects during the first test trial than during the second test trial. On the contrary, following habituation with a smooth object, whatever the held object during test trials (new or familiar) latepreterm neonates held objects longer during the second test trial than during the first test trial, (p ¼ .008). In order to determine whether or not late-preterm neonates really failed to detect the new granular object

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after being habituated to the smooth object we calculated a detection score. For each late-preterm neonate, detection score was calculated by subtracting the mean holding time during the two test trials from the mean holding time during the two last habituation trials. This index is a measure of the amount of change in holding time, from habituation to test period, relative to each subject’s own habituated holding level. A 2 (Habituation object: smooth vs. granular)  2 (Test object: new vs. familiar) ANOVA was performed on detection score. ANOVA failed to reveal a significant effect of the Habituation object, F(1, 28) ¼ .03, p ¼ .86, a ¼ .05, of the Test object, F(1,28) ¼ .02, p ¼ .90, a ¼ .05 nor of the Habituation object  Test object interaction, F(1, 28) ¼ 1.25, p ¼ .27, a ¼ .19.

Holding Time Analysis During Test Period in Early-Term Neonates Test trials of early-term infants were also analyzed with a 2  2  2 mixed-model ANOVA with Habituation object (smooth vs. granular) and Test object (new vs. familiar) as between subjects factors and with Trials (first and second test trials) as a within subjects factor (Figure 2). ANOVA performed on test period failed to reveal a significant effect of the Habituation object, F (1, 28) ¼ .02, p ¼ .89, a ¼ .05, the Test object, F(1, 28) ¼ .60, p ¼ .44, a ¼ .11 nor of the Trials, F(1, 28) ¼ .01, p ¼ .91, a ¼ .05. ANOVA only revealed a significant Habituation object  Test object interaction F(1,28) ¼ 8.54, p ¼ .006, a ¼ .80). Planned comparisons were performed to analyze this interaction and revealed that after habituation to the smooth object, holding times during test trials were higher for neonates holding the new granular object (M ¼ 18.74 s, SD ¼ 20.21) than for neonates holding the familiar smooth object (M ¼ 2.73 s, SD ¼ 1.65), F(1, 28) ¼ 4.75, p ¼ .037. However, although after habituation to the granular object, holding times during test trials were higher for neonates holding the new smooth object (M ¼ 15.99 s, SD ¼ 10.61) than for neonates holding the familiar granular object (M ¼ 6.71 s, SD ¼ 8.63), the difference was not significant, F(1, 28) ¼ 1.80, p ¼ .18. No other significant interactions were observed. The question still remains to determine whether or not early-term neonates really detected the new granular object after being habituated to the smooth object. A 2 (Habituation object: smooth vs. granular)  2 (Test object: new vs. familiar) ANOVA was performed on detection score calculated for early-term neonates. Analysis failed to reveal a significant effect of the Habituation object, F(1, 28) ¼ .13, p ¼ .72, a ¼ .06, the Test object, F(1, 28) ¼ .12, p ¼ .74, a ¼ .06. A significant Habituation object  Test object interaction

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was observed, F(1, 28) ¼ 10.35, p ¼ .003, a ¼ .88. Planned comparisons were performed to investigate further this interaction. Following habituation with the granular object, detection score was significantly higher, F(1, 28) ¼ 4.21, p ¼ .05, for the new smooth object (M ¼ 12.37 s, SD ¼ 10.55) than for the familiar granular object (M ¼ 1.39 s, SD ¼ 6.20). Following habituation with the smooth object, detection score was significantly higher, F(1, 28) ¼ 6.34, p ¼ .018, for the new granular object (M ¼ 12.33 s, SD ¼ 17.6) than for the familiar smooth object (M ¼ 1.27 s, SD ¼ 2.5). This analysis clearly revealed that early-term neonates reacted to a change in object texture whatever the object they were habituated to.

Hand Pressure Frequency Habituation Period. Table 5 summarizes total HPF all over the habituation period, HPF during the first two trials, and HPF during the last two trials for both groups of infants and for both objects. Infants’ hand pressure frequency (in Hz) during habituation trials was analyzed with a 2  2  4 mixedmodel ANOVA with Groups (early-term vs. latepreterm), Habituation objects (smooth vs. granular) as a between subjects factors and with Trials (First, second, second last, and last trials of habituation) as a within subjects factor. The main effect of the Group was not significant, F(1, 60) ¼ 1.62, p ¼ .20 a ¼ .24. A main effect of the Trials was observed, F(3, 180) ¼ 5.70, p < .001, a ¼ .94 revealing that hand pressure frequency decreased as habituation progressed. The habituation phenomenon was not equally shared among the two groups of neonates as revealed by a significant Trials  Group interaction, F(3, 180) ¼ 3.99, p ¼ .009, a ¼ .83 (Fig. 3). Fisher post hoc comparisons indicated that in late-preterm neonates, the mean hand pressure frequency recorded for the first trial of habituation (M ¼ .17 Hz, SD ¼ .19) did not differ from the second last (M ¼ .16 Hz, SD ¼ .24, p ¼ .88) and the

last trial of habituation (M ¼ .14 Hz, SD ¼.17, p ¼.67). Similarly, the mean hand pressure frequency during the second trial of habituation (M ¼.17 Hz, SD ¼ .20) did not differ from the second last (p ¼ .85) and the last trial of habituation (p ¼ .78). On the contrary, Fisher post hoc comparisons indicated that in early-term neonates, the mean hand pressure frequency during the first trial of habituation (M ¼ .28 Hz, SD ¼ .28) differed from the second last (M¼ .12 Hz, SD ¼.19, p ¼.01) and the last trial of habituation (M ¼.07 Hz, SD ¼ .15, p ¼ .0009). Similarly, the mean hand pressure frequency during the second trial of habituation (M ¼ .36 Hz, SD ¼ .51) differed from the second last (p < .001) and the last trial of habituation (p < .0001). These results underlined that, in early-term neonates, hand pressure frequency decreased with repetition of trials, testifying of an habituation process. On the contrary, this phenomenon was not observed in late-preterm neonates for whom hand pressure frequency remained unchanged over the repetition of trials. ANOVA also revealed a significant effect of the Habituation objects, F(1, 60) ¼ 5.74, p ¼ .002, a ¼ .65, suggesting that hand pressure frequency was higher for a smooth (M ¼ .25 Hz, SD ¼ .28) than for a granular object (M ¼ .15 Hz, SD ¼ .09). However, as revealed by a significant Habituation object  Group interaction, F (1, 60) ¼ 6.25, p ¼ .02, a ¼ .69, modulation of hand pressure frequency according to the texture of objects differed across groups of neonates (Fig. 3). Fisher post hoc comparisons indicated that in early-term neonates, mean hand pressure frequency was significantly higher (p < .001) for a smooth (M ¼ .35 Hz, SD ¼ .35) than for a granular object (M ¼ .13 Hz, SD ¼ .06). On the contrary, Fisher post hoc tests indicated that in latepreterm neonates, mean hand pressure frequency was not significantly higher (p ¼ .94) for a smooth (M ¼ .16, SD ¼ .13) than for a granular object (M ¼ .17, SD ¼ .11). These results clearly revealed that, contrary to late-preterm neonates, early-term neonates modulate hand pressure frequency according to object texture.

Table 5. Total Hand Pressure Frequency (in Hz), Hand Pressure Frequency (in Hz) During the First Two Trials, and During the Last Two Trials (in Hz) According to Groups (Early-Term vs. Late-Preterm) and Objects (Smooth vs. Granular). SDs are Given Into Brackets

Groups Early-Term (N ¼ 32) Late-Preterm (N ¼ 32)

Habituation Object Smooth (N ¼ 16) Granular (N ¼ 16) Smooth (N ¼ 16) Granular (N ¼ 16)

HPF (Hz) Throughout the Habituation Period 2.67 0.91 0.92 0.83

(.38) (.46) (.68) (.47)

HPF (Hz) During the First Two trials .98 .29 .35 .31

(.81) (.26) (.29) (.28)

HPF (Hz) During the Last Two trials .20 .18 .28 .31

(.32) (.17) (.42) (.27)

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FIGURE 3 Hand Pressure Frequency in Hz (mean and standard error) for granular (left part of the graph) and smooth (right part of the graph) objects during the 4 trials of the habituation period and the 2 test trials for late-preterm (upper part of graph) and early-term infants (lower part of graph).

Test Period Hand pressure frequency (in Hz) during test trials was analyzed with a 2  2  2  2 mixed-model ANOVA with Groups (early-term vs. late-preterm), Habituation objects (smooth vs. granular) and Test objects (new vs. familiar) as between Subjects factors and with Trials (first and second test trials) as a within Subjects factor. ANOVA failed to reveal a significant effect of the Group, F(1, 56) ¼ .32, p ¼ .57, a ¼ .08, the Habituation object, F(1, 56) ¼ .58, p ¼ .08, a ¼ .08, the Test object, F(1, 56) ¼ .79, p ¼ .37, a ¼ .14 and the Trials, F(1, 56) ¼ .02, p ¼ .89, a ¼ .05. A significant Habituation object  Test object interaction was observed, F(1, 56) ¼ 38.64, p < .00001, a ¼ .99 (Fig. 3). Planned comparisons were performed to analyze this interaction. Following habituation with the granular object, hand pressure frequency was significantly higher, F(1, 56) ¼ 25.20, p < .0001, for the new smooth (M ¼ .36 Hz, SD ¼ 1.22) than for the familiar granular object

(M ¼ .08 Hz, SD ¼ .12). Following habituation with the smooth object, hand pressure frequency was significantly higher, F(1, 56) ¼ 14.13, p < .001, for the new granular (M ¼ .3 Hz, SD ¼ .2) than for a familiar smooth object (M ¼ .09 Hz, SD ¼ .15). However, as revealed by a significant Group  Habituation object  Test object interaction, F(1, 56) ¼ 17.03, p < .01, a ¼ .98, the increase of hand pressure frequency during test period for the new textured-object was not observed in both groups of neonates. Fisher post hoc comparisons were conducted to analyze this unexpected Group  Habituation object  Test object interaction. Analyses showed that in latepreterm neonates, following habituation with the granular object, mean hand pressure frequency during test period was not significantly higher (p ¼ .45) for the new smooth (M ¼ .20 Hz, SD ¼ .11) than for the familiar granular object (M ¼ .15 Hz, SD ¼ .14). Similarly, mean hand pressure frequency was not significantly higher (p ¼ .19) for the new granular object

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(M ¼ .27 Hz, SD ¼ .24) than for the familiar smooth object (M ¼ .17 Hz, SD ¼ .19) after habituation with the smooth object. Pattern of results was somewhat different in early-term neonates. Mean hand pressure frequency recorded during the test period after habituation with the granular object was significantly higher (p < .00001) for the new smooth object (M ¼ .52 Hz, SD ¼ .19) than for the familiar granular object (M ¼ .01 Hz, SD ¼ .04). Following habituation with the smooth object, mean hand pressure frequency was also significantly higher (p < .00001) for the new granular object (M ¼ .33 Hz, SD ¼ .16) than for the familiar smooth object (M ¼ .02 Hz, SD ¼ .05). Taken together results revealed that early-term neonates increased hand pressure frequency for the new textured object but not for the familiar textured object. This reaction was not observed in late-preterm neonates who did not exhibit higher hand pressure frequency for the new texturedobject when compared to the familiar textured-object. The latter result raised the question to know whether or not late-preterm infants noticed the change of the new object after habituation with the familiar textured object. To answer this question, detection score was also calculated for hand pressure frequency by subtracting the mean pressure frequency during the two test trials from the mean pressure frequency during the two last habituation trials. A 2 Group (early-term vs. latepreterm)  2 Habituation object (smooth vs. granular)  2 Test object (new vs. familiar) ANOVA was performed on detection score. ANOVA performed on detection score failed to reveal a significant effect of the Group, F(1, 56) ¼ 2.84, p ¼ .09, a ¼ .38, the Habituation object, F(1, 56) ¼ .17, p ¼ .68, a ¼ .06, the Test object, F(1, 56) ¼ 1.12, p ¼ .29, a ¼ .18. A significant Habituation object  Test object interaction was observed, F(1, 56) ¼ 52.50, p < .000001, a ¼ 1. Planned comparisons performed to analyze this interaction revealed that following habituation with the granular object, detection score was significantly higher, F(1, 56) ¼ 19.15, p < .0001, for the new smooth (M ¼ .23 Hz, SD ¼ .23) object than for the familiar granular object (M ¼ .04 Hz, SD ¼ .13). Following habituation with the smooth object, detection score was significantly higher, F(1, 56) ¼ 34.48, p < .0001, for the new granular (M ¼ .26 Hz, SD ¼ .17) than for the familiar smooth object (M ¼ .11 Hz, SD ¼ .21). However, as revealed by a significant Group  Habituation object  Test object interaction, F(1, 56) ¼ 8.12, p ¼ .006, a ¼ .80, both groups of infants differed for detection scores. Fisher post hoc test revealed that detection scores of early-term neonates were significantly higher (p < .00001) for the new smooth object (M ¼ .40 Hz, SD ¼ .18) than for the

Developmental Psychobiology

familiar granular object (M ¼ .05 Hz, SD ¼ .06) after habituation with the granular object. Similarly, after habituation with the smooth object, detection scores of early-term infants were also significantly higher (p < .00001) for the new granular object (M ¼ .30 Hz, SD ¼ .15) than for the familiar smooth object (M ¼ .15 Hz, SD ¼ .23). This was different for late-preterm neonates. Post hoc comparisons revealed that in latepreterm neonates, detection scores recorded for the new smooth (M ¼ .06 Hz, SD ¼ .15) and for the familiar granular object (M ¼ .03 Hz, SD ¼ .18) did not vary (p ¼ .27) after habituation with the granular object. But on the contrary, following habituation with the smooth object, detection scores were significantly higher (p ¼ .002) for the new granular object (M ¼ .23 Hz, SD ¼ .2) than for the familiar smooth object (M ¼ .07 Hz, SD ¼ .21).

DISCUSSION The first purpose of this study was to analyze the onset of active touch in preterm infants. Using habituation paradigm, two groups of neonates varying according to gestational age in weeks (34 GW and 38 GW) but matched for experiential age (3–6 days) were systematically compared when they held textured-objects. First result is that both populations exhibit habituation to granular and smooth textures as demonstrated by holding time analysis. Regardless of the texture of objects, both patterns of habituation are comparable, though differences exist across participants with latepreterm infants requiring more time to get habituated than early-term neonates. This result gives some support to previous works concluding to haptic habituation to texture in full-term neonates (Molina & Jouen, 2004) and to shape of object in preterm neonates (Lejeune et al., 2010, 2014; Marcus, Lejeune, BerneAude´oud, Gentaz, & Debillon 2012). The second important result is that the ability to react to a new object differs in late-preterm and earlyterm neonates. As a matter of fact, the analysis of holding time, during the test period, failed to reveal that late-preterm neonates presented with a new object held longer the object than late-preterm neonates presented with a familiar object. Furthermore, the detection score did not reveal that holding times were significantly modified from habituation to test period. The analysis of HPF during habituation and test periods allows understanding the failure of late-preterm neonates to demonstrate reaction to novelty. During habituation, HPF was low and similar for both smooth and granular objects. Moreover, HPF was not modified by the repetition of habituation trials and remained

Developmental Psychobiology

remarkably stable over time. This underlines that any modulation of HPF was observed during habituation and for different textures, suggesting that late-preterm neonates do not actively explore objects and do not use hand to pick up information about texture. A direct consequence of the absence of active exploration during habituation period is that late-preterm neonates were unable to process the novelty of the object during the test period. This is confirmed by the data: Hand pressure frequency was not modulated according to the degree of familiarity of the previously held object. Whatever the granular or smooth object proposed during habituation, HPF of late-preterm infants presented with a new-textured object was not significantly different than HPF recorded in neonates presented with a familiar object. Absence of active exploration could also explain the absence of difference in holding time across late-preterm neonates presented with a new or a familiar object during the test period. Alternative explanation would hold that the absence of object exploration is related to tiredness or hypotonia. This plausible interpretation does not fit with the obtained data: After habituation late-preterm neonates always tend to hold longer new objects, although this increase is not significant. As underlined in result section, the non-significant reaction to novelty could be related to the fluctuation of holding times during the two test trials. It could also be objected that late-preterm infants failed in perceiving texture of objects. This interpretation seems contradictory with the fact that greater HPF detection score was observed in late-preterm infants after habituation to a smooth object when a new granular was presented. This clearly indicates that latepreterm infants are able to notice the change in the object texture. However this ability seems densitydependent since such detection was not observed when after habituation to the granular object the smooth object was presented. As described in the method section, both objects used in the present experiment differ in terms of the density of texture with a lower density for the smooth than for the granular object. Many researches have demonstrated that young infants are more responsive to quantitative than to qualitative aspects of stimulation (e.g., McGuire & Turkewitz, 1978; Turkewitz, Lewkowicz, & Gardner, 1983). For example, Lewkowickz and Turkewitz (1981) have established that the perception of a change in the intensity depends on the features of the stimulation and on the characteristics of the organism such as the arousal level or the adaptive state of peripheral receptors. Authors explain that a light with a particular brightness might be effectively intense for an infant who is dark-adapted but effectively weak for an infant who is adapted to light. Similar reasoning can be used

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for the textured-objects. The granular object is probably perceived by neonates adapted to the lower density smooth object, as intense and then induces an increased HPF. On the contrary, the low-density smooth object when presented after repeated exposition to a higher intense granular object is perceived as weak, and in consequence is insufficient to induce a reaction in neonates adapted to a high-density object. A different pattern of results is observed in earlyterm neonates. First of all, holding time analysis reveals that, whatever the object (smooth or granular) they were habituated to, neonates were able to react to the presentation of a new textured-object: After habituation, early-term neonates presented with a new object, increased holding time contrary to neonates presented with the familiar object. This reaction to novelty clearly reveals that early-term neonates identify the change that occurred in texture between habituation and test periods. This is confirmed by the HPF analysis that also demonstrates that, whatever the test-object (smooth or granular), pressure frequency was increased for a new object. On the contrary, such increase was not observed when the familiar object of the habituation period continued to be presented during the test period. Second, unlike late-preterm infants in whom any change of HPF was detected during habituation, earlyterm neonates modulate HPF in reference to the repetition of habituation trials. This modulation of manual activity clearly suggests that early-term neonates exhibit exploratory dynamic process that evolves according to time and allows the perception and the processing of texture of objects. When exploring objects early-term neonates use active touch since they develop specific patterns of movements according to the different textures with significant higher HPF for smooth texture than for granular texture. This pattern of results observed for early-term infants is very closed to different data reported in full-term neonates and concluding to a modulation of hand activity according to object property (see for a review, Jouen & Molina, 2005). However, early-term neonates exhibit only one slight difference when compared to full-term infants (Molina & Jouen, 2004). Contrary to full-term infants, early-term neonates do no hold significantly longer a new textured-object after being habituated to a granular object. The logic of this experiment in which neonates of different gestational age and matched for postnatal experience allows us to tackle the question of the onset of active touch perception for texture. At mean age of 34 GW, infants use passive touch that is not irreconcilable with the fact that they exhibit habituation. As stressed out by Gibson (1962); “passive touch involves only the excitation of receptors in the skin and its

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underlying tissue.” The simple repetition of the stimulation is thus sufficient to induce a significant reduction of holding time according to general principal of habituation in individuals. However around 34 GW, infants do not exhibit significant reaction to novelty for texture. At a mean age of 38 GW, neonates are able to use active touch when habituated to objects varying in texture and to react to new textured object even if the reaction to novelty is slightly different from what is observed in full-term infants. Since post-natal experience was maintained constant in both groups of infants, our results clearly demonstrate that the transition from passive to active touch for texture exploration that occurs between 34 and 38 weeks is associated to maturation processes. Our results contrast with previous data that reported active touch of preterm for shape (Lejeune et al., 2010). These discrepancies may raise from the investigated object property that is different: Texture and shape could be differently processed in preterm infants as it has been demonstrated in full-term neonates (Sann & Streri, 2007, 2008). Nevertheless, our results are congruent with different studies that have documented the immaturity of the preterm infant’s brain and demonstrated different organization of cerebral connections in preterm infants when compared to full-term infants (Smyser, Synder, & Neil, 2011). Results are also congruent with recent evidences (Sengupta et al., 2013) that have pointed toward immaturity and particular neonatal outcomes with early-term birth (37–38 GW) compared with full-term neonates (39–41 GW).

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Developmental Psychobiology Humphrey, T. (1970). The development of human fetal activity and its relation to postnatal behaviour. Advances in Child Development and Behavior, 5, 1–57. Jouen, F., & Molina, M. (2005). Exploration of the newborn’s manual activity: a window onto early cognitive processes. Infant Behavior and Development, 28, 227–239. Jouen, F., Sann, C., & Molina, M. (2012). Haptic Processing in newborns of depressed and nondepressed mothers. Developmental Psychiobiology, 54(4), 451–459. Kandel E. R., Schwartz J. H., & Jessell T. M. (2000). Principles of Neuroscience. 4th ed. New York: McGrawHill. Lederman, S. J., & Klatzky, R. L. (1987). Hand movements: A window into haptic object recognition. Cognitive Psychology, 19, 342–368. Lejeune, F., Audeoud, F., Marcus, L., Streri, A., Debillon, T., & Gentaz, E. (2010). The manual habituation and discrimination of shapes in preterm human infants from 33 to 34 þ 6 post-conceptional age. Plos ONE, 5(2), e9108. Lejeune, F., Marcus, L., Berne-Aude´oud, F., Streri, A., Debillon, T., & Gentaz, E. (2012). Inter-manual transfer of shapes in preterm human infants from 33 to 34þ6 weeks post-conceptional age. Child Development, 83, 794–800. Lejeune, F., Berne-Audeoud, F., Marcus, L., Debillon, T., & Gentaz, E. (2014). The effect of postnatal age on the early tactile manual abilities of preterm infants. Early Human Development, 90, 259–264. Lewkowicz, D. J., & Turkewitz, G. (1981). Intersensory interaction in newborns: Modification of visual preferences following exposures to sound. Child Development, 52, 827–832. Marcus, L, Lejeune, F, Berne-Aude´oud, F, Gentaz, E, & Debillon, T. (2012). Tactile sensory capacity of the preterm infant: manual perception of shape from 28 gestational weeks. Paediatrics, 130(1), 88–94. McGuire, I., & Turkewitz, G. (1978). Visually elicited finger movements in infants. Child Development, 49, 362–370. Mento, G., & Bisiachi, P. S. (2012). Neurocognitive development in preterm infants: insights from different approaches. Neuroscience and Biobehavioral Reviews, 36(1), 536–555. Molina, M., & Jouen, F. (1998). Modulation of palmar grasp behavior in neonates according to texture property. Infant Behavior and Development, 21(4), 659–666. Molina, M., & Jouen, F. (2003). Haptic intramodal comparison of texture in human neonates. Developmental Psychobiolgy, 42(4), 378–385. Molina, M., & Jouen, F. (2004). Manual cyclical activity as an exploratory tool in neonates. Infant Behavior and Development, 27(1), 42–53. Nevalainen, P., Lauronen, L., & Pihko, E. (2014). Development of human somatosensory cortical functions – what have we learned from magnetoencephalography: a review. Frontiers in Human Neurosciences, 8(158), 1–15. Rochat, P. (1987). Mouthing and grasping in neonates: evidence for the early detection of what hard or soft substances afford for action. Infant Behavior and Development, 10(4), 435–449.

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Smyser, C. D., Inder, T. E., Shimony, J. S., Hill, J. E., Degnan, A. J., Snyder, A. Z., & Neil, J. J. (2010). Longitudinal analysis of neural network development in preterm infants. Cerebral Cortex, 20, 2852–2862. Smyser, C. D., Synder, A.Z, & Neil, J.J (2011). Functional connectivity MRI in infants: Exploration of the functional organization of the developing brain. Neuroimage, 56(3), 1437–1452. Streri, A., Lhote, M., & Dutilleul, S. (2000). Haptic perception in newborns. Developmental Science, 3(3), 319–327. Turkewitz G., Lewkowicz D. J., & Gardner J., (1983). Determinants of infant perception. In: J. Rosenblatt, C. Beer, R. Hinde, & M. Busnel, (Eds.), Advances in the study of behavior pp. 39–62. New York: Academic, Vol. 13.