Research in Developmental Disabilities 34 (2013) 4546–4558

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Research in Developmental Disabilities

The effect of a short bout of practice on reaching behavior in late preterm infants at the onset of reaching: A randomized controlled trial Daniele de Almeida Soares a,1,*, John van der Kamp b,c, Geert J. Savelsbergh b, Eloisa Tudella a a

Department of Physical Therapy, Neuropediatrics Section, Federal University of Sa˜o Carlos (UFSCar), Rod Washington Luis, km 235, 13565-905 Sa˜o Carlos, SP, Brazil Research Institute MOVE, Faculty of Human Movement Sciences, Vrije Universiteit (VU Amsterdam), Van der Boechorststraat 9, 1081 BT Amsterdam, The Netherlands c Institute of Human Performance, University of Hong Kong, Sassoon Road, Hong Kong Special Administrative Region b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 16 July 2013 Received in revised form 14 September 2013 Accepted 19 September 2013 Available online 18 October 2013

The purpose of this study was to examine the effects of a short bout of practice on reaching behavior in late preterm infants at the onset of goal-directed reaching. The study was designed as a blind, three-arm parallel-group, randomized controlled, clinical trial. Thirtysix late preterm infants were recruited from a maternity hospital and allocated according to computer generated randomization into groups that received reaching practice based on either a blocked schedule, a serial schedule, or no practice. Practice consisted of a 4 min session of induced reaching using a toy in three activities guided by a physical therapist. The activities were elicited in separate blocks for the blocked practice group and in a preestablished order for the serial practice group. The control group stayed in the physical therapist’s lap but was not stimulated to reach. The infants were assessed 3.3  1.4 days after the onset of goal-directed reaching in three tests: pre-test (immediately before practice), post-test (immediately after practice), and retention test (24 h after post-test). During assessments, the infants were seated in a baby chair and a toy was presented at his/her midline within reaching distance for 2 min. Changes in the number of reaches, proportions of uni/ bimanual reaches and kinematic parameters of reaching were main outcome measures. From pre- to post-test, the amount of reaches and bimanual reaches increased in the serial practice group, but the increase was not maintained in the retention test. Kinematic parameters were not affected by practice. Changes in the reaching behavior of late preterm infants can be triggered after the first few minutes of toy-oriented experience based on a serial practice schedule. These changes are not consolidated one day later. ß 2013 Elsevier Ltd. All rights reserved.

Keywords: Movement training Reaching behavior Premature birth Motor learning

1. Introduction Infants are naturally interested in the world around them and are constantly discovering new ways to interact with it. As goal-directed reaching emerges, around 3–4 months of age (Thelen et al., 1993; von Hofsten, 1979), the possibilities for exploring the environment enlarges dramatically (Lobo & Galloway, 2013a). Hence, infants increasingly improve their ability

* Corresponding author at: Rua Vitor Manoel de Souza Lima, 328/17, Vila Pureza, 13561-020 Sa˜o Carlos, SP, Brazil. Tel.: +55 1633518407. E-mail address: [email protected] (D.d.A. Soares). 1 This author and this study were financially supported by the Sa˜o Paulo Foundation for Research Support (FAPESP), Brazil. 0891-4222/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ridd.2013.09.028

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to act upon and experience objects. This developmental path, however, may not always be typical for infants at risk for developmental delays, such as infants that are born preterm. There is growing body of evidence that preterm infants show differences in comparison to typically developing infants in the amount of reaching and their organization. There are indications that preterm infants show different developmental patterns in proximal (e.g., the distribution of uni- and bimanual reaches) and distal control (e.g., the changes in hand opening) and reaching kinematics (e.g., movement velocity, movement units, etc.) (see Guimara˜es, Cunha, Soares, & Tudella, 2013, for a review). For example, relative to typically developing infants, preterm infants born at less than 33 weeks of gestational age show a delayed reaching onset (Fallang, Saugstad, & Hadders-Algra, 2003; Heathcock, Lobo, & Galloway, 2008) and perform less reaches and reaches with more nonfunctional hand postures (i.e., closed) once they acquire reaching (Heathcock et al., 2008). In addition, preterm infants with less than 32 weeks of gestation use more bimanual than unimanual reaches when reaching for moving objects at 8 months corrected age. This prevalence of bimanual reaching may be a strategy for maximizing reaching range and thus suggestive for preterm infants being less skilled reachers than fullterm infants (Gro¨nqvist, Strand Brodd, & von Hofsten, 2011). Yet, it is still unknown which proximal strategy preterm infants adopt to reach for stationary objects at or shortly after reaching onset. These infants also reach with less velocity and more movement units compared to full-term infants at 4–6 months corrected age. This may reflect a dysfunction in the ability to modulate the movement (Fallang et al., 2003; Fallang, Øien, Hellem, Saugstad, & Hadders-Algra, 2005). It is unclear yet how this kinematic control in preterm infants is characterized at or shortly after reaching onset. Also the reaching in late preterm infants (i.e., born at 34–36 6/7 weeks of gestation) shows differences with full-terms. Although it is not known if reaching is delayed or less frequent compared to typically developing infants, they do show differences in the control of fingers and hand movements at 6 months corrected age by more often reaching with an open hand. Late preterm infants reach with lower velocities and spend more time decelerating their arm movement prior to contact with the object (Toledo, Soares, & Tudella, 2011; Toledo & Tudella, 2008). Again, at present, the organization of reaching at onset is unclear, but these differences relative to full-term infants might present a constraint for further learning and the acquisition of fine manipulative skills that may only become apparent in later years (Fallang et al., 2005). Hence, exploring early reaching interventions to minimize these constraints is evidently of relevance. Interestingly, as far as we know, there is only one study that investigated the role of movement practice in an early preterm population (born < 33 weeks of gestation; Heathcock et al., 2008), but none that examined practice in late preterm infants. Heathcock et al. (2008) found that after 4–8 weeks of daily practice of hand–toy interaction applied by parents and initiated before reaching onset, the preterm infants started reaching at the toy at younger age and showed enhanced quantity and quality of reaching, in particular for distal control (i.e., more reaches with open and a ventrally oriented hand) relative to untrained preterm infants. However, Heathcock et al. (2008) did not specify the nature of practice. Hence, we raise two questions. Does a short bout of practice (i.e., a few minutes) affect the reaching behavior of newly-reaching late preterm infants as well, and if so, are these changes dependent on the scheduling of practice? Physical and occupational therapists often experience immediate changes in the motor behavior of preterm infants after only few minutes of social and sensori-motor stimulation (e.g., enticing infants with a toy). Nevertheless, research on effects of short motor practice in preterm infants to confirm these subjective observations are lacking. In full-term infants who just started reaching, it has been recently demonstrated that 4 min of practice produced an immediate increase in the number of reaches, enhanced proximal (more unimanual reaches) and distal control (more reaches with semi-open hand) and shorter and faster reaches compared to baseline measures (Cunha, Soares, Ferro, & Tudella, 2013; Cunha, Woollacott, & Tudella, 2013). Similar to findings in adults after motor practice in the order of magnitude of minutes (Karni et al., 1995), these immediate effects are likely granted by the plasticity of the infant brain (e.g., Kolb & Gibb, 2011; Mackey, Whitaker, & Bunge, 2012), although this has not been confirmed for motor behavior. Practice is often scheduled in blocked (e.g., 111–222–333), random (e.g., 213–123–132) or serial (e.g., 123–123–123) sequences of similar movements or tasks (Schmidt & Wrisberg, 2008). In adults, random and serial schedules generate higher contextual interference than blocked schedule, that is, they disrupt the performance of an activity, but paradoxically results in better retention (Battig, 1979; Shea & Morgan, 1979; also see Magill & Hall, 1990, for a review). In children, studies are relatively scarce and the results ambiguous (e.g., Pigott & Shapiro, 1984; Ste-Marie, Clark, Findlay, & Latimer, 2004; Zetou, Michalopoulou, Giazitzi, & Kioumourtzoglou, 2007). However, some have argued that contrary to adults, in children, whose motor and cognitive abilities are still maturing (Bell & Wolfe, 2007; Zipp & Gentile, 2010), low contextual interference would be more advantageous for learning (Jarus & Goverover, 1999; Pigott & Shapiro, 1984). This is based on the idea that low contextual interference adds less extrinsic variability and, therefore, requires less effort to assemble suitable movement patterns (Zipp & Gentile, 2010) and to elaborate memory representations for the to-be-learned task (Battig, 1979; Magill & Hall, 1990) compared to higher contextual interference. In this sense, the learning of motor skills in young children and children with compromised memory processes seems to be favored by practice techniques that require less use of cognitive demands. As preterm infants can present difficulties in working memory and learning processes early in infancy (Gekoski, Fagen, & Pearlman, 1984; Heathcock, Bhat, Lobo, & Galloway, 2004; Jongbloed-Pereboom, Janssen, Steenbergen, & Nijhuisvan der Sanden, 2012) and later acquisition of motor skills may be related to such difficulties (Lobo & Galloway, 2013b; Steenbergen, van der Kamp, Verneau, Jongbloed-Pereboom, & Masters, 2010), contextual interference in the motor behavior of preterm infants is an issue that deserves research. In this study, we investigated the role of late prematurity and contextual interference on early reaching behavior. Specifically, we assessed immediate and delayed (i.e., after 24 h) effects induced by few minutes of reaching practice under

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blocked or serial sequences on the amount of reaching and its organization (i.e., proximal and distal control and kinematic characteristics) in late preterm infants at the onset of the skill. We hypothesized that toy-oriented repetition of reaching movements for 4 min can enhance the reaching behavior of late preterm infants at the onset of the skill. Thus, we predicted that immediately after practice, the infants would enhance the amount of reaching, proximal adjustments (i.e., more uni-, less bimanual reaches), distal adjustments (i.e., more reaches with open hand) and reaching kinematics (reaches with less movement units, less deceleration time and higher velocity). Secondly, because high contextual interference can increase motor perturbation (Zipp & Gentile, 2010) and the demands of cognitive abilities for task strategies (Magill & Hall, 1990) during skill acquisition, we hypothesized that late preterm infants at reaching onset benefit more from practice under lower than higher contextual interference. Hence, we expected that immediately after practice enhancement of proximal/distal adjustments and kinematics of reaching would be greater in the infants who received blocked practice than in those who received serial practice. Further, we hypothesized that enhancement of proximal/distal adjustments and kinematics of reaching 24 h after practice would be greater in the blocked practice than in the serial practice group.

2. Materials and methods 2.1. Participants This study included 36 late preterm infants (M = 35.3  0.9, weeks of gestation), aged from 2.5 months of chronological age at the beginning of their participation, discharged from hospital, adequate to gestational age (WHO, 1995) (Table 1), with mean score of 12.5  1.3 according to the Alberta Infant Motor Scale (AIMS; Piper & Darrah, 1994), and able to perform at least three reaches in the baseline assessment at the laboratory (pre-test). Infants who showed at least one of the following conditions, according to medical records and/or their neonatologist’s report, were excluded from the study: (a) anoxia, (b) signs of neurological complications (e.g., convulsions, intracranial hemorrhage and any changes in cerebral ultrasound), (c) hyperbilirubinemia, (d) congenital malformations (e.g., congenital foot deformity), (e) Down syndrome, (f) visual or auditory alterations, (g) cardiopulmonary difficulties, (h) intra-uterine or post-natal growth restriction, and (i) admission to Neonatal Intensive Care Unit. The infants were recruited from the maternity hospital of the city of Sao Carlos, state of Sao Paulo (Brazil) and were assessed at the Laboratory of Research in Movement Analysis of the Department of Physical Therapy, Federal University of Sao Carlos. The study was approved by the Ethics and Research Committee (protocol no. 111/2011) of the University. Prior informed legal consent was obtained from the participants’ parents. 2.2. Apparatus Infant allocation to one of three treatment groups was performed using the software Mathematica to generate computer randomization. Allocation was concealed from researchers and parents in sequentially numbered, opaque, sealed envelopes. Infants were assessed in a baby chair reclined 458 from the floor with back long enough to include a headrest. A malleable rubber toy (5.0 cm smaller diameter, 12.0 cm larger diameter, 10.0 cm height) was used to elicit reaching. Two reflexive markers (5 cm diameter) were used to track the reaching movements. A small pillow was used to support the infant’s head during practice protocols (Cunha, Soares, et al., 2013; Cunha, Woollacott, et al., 2013). The assessments were recorded using a four-camera (60 Hz) motion capture system (Dvideow 5.0; Figueroa, Leite, & Barros, 2003). One camera was positioned posterior-superiorly to the infant and other two were positioned posteriorlaterally to the infant – one to the right and one to the left side. Thus, the markers were visible throughout the reaching movements. A forth camera was positioned anterior-laterally to the infant in order to clarify doubts related to the visualization of the movements. The system displayed x, y and z coordinates from the markers fixed to each wrist for each frame of the movement. Matlab routines were used to filter these data through a fourth-order Butterworth filter (cutoff frequency of 6 Hz) and to calculate the kinematic variables (Carvalho, Tudella, & Savelsbergh, 2007). The categorical variables were coded using synchronized images from the cameras in a monitor.

Table 1 Characteristics of the sample (mean and standard deviation) by group. Characterization

Blocked practice

Serial practice

Control

py

Gestational age (weeks) Birth weight (kg) Actual weight (kg) Actual length (cm) Apgar 1st min Apgar 5th min Number of days after reaching onseta

35.4  0.9 2.7  0.4 6.0  1.1 60.4  3.0 8.8  0.8 9.7  0.4 3.0  1.3

35.3  0.8 2.5  0.3 6.11  0.6 60.7  2.4 8.7  0.9 9.7  0.6 3.6  1.5

35.1  0.9 2.3  0.3 5.9  0.8 59.7  2.0 8.3  1.0 9.4  0.7 3.2  1.3

0.7 0.4 0.9 0.6 0.3 0.4 0.6

a y

Number of days up to the pre-test in the laboratory after confirmation of reaching onset. p-Value from ANOVA One-Way indicating homogenous characteristics between groups.

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Table 2 Protocols of reaching practice. Activity 1

Activity 2

Activity 3

The physical therapist held the toy in one hand, at the infant’s midline and xiphoid process height. With the other hand, the physical therapist held the forearm of the infant in order to lead the hand toward the toy resulting in touching it

The physical therapist held the toy in one hand, at the infant’s midline and xiphoid process height. With the other hand, the physical therapist held the forearm of the infant in order to position the hand within his/her visual field for a few seconds. The physical therapist waited a few seconds to allow the infant to move his/her hand closer to the toy to touch it actively. If the infant did not touch the toy spontaneously, the physical therapist performed tactile stimuli with the toy in the hand of the infant

The upper limb of the infant was positioned along his/her body. The physical therapist performed tactile stimuli with the toy along the arm, forearm and hand of the infant and took the toy to the infant’s midline, at his/her xiphoid process height, within his/her visual field. The physical therapist waited a few seconds to allow the infant to perform active uni or multi-joint movements of the upper limb. If the infant touched the toy, the physical therapist, with a smile, praised him/her (‘‘Good job!’’). If the infant tried to grasp the toy, the physical therapist let him explore it for a few seconds

Practice based on blocked schedule: 111(R)–111(L)–222(R)–222(L)–333(R)–333(L) Practice based on serial schedule: 123(R)–123(L)–123(R)–123(L)–123(R)–123(L). 1, activity 1; 2, activity 2; 3, activity 3; R, right hand/arm; L, left hand/arm.

2.3. Procedure and design This is a blind, three-arm parallel-group, randomized controlled, clinical trial (Brazilian Clinical Trials Registry, protocol no. RBR-2DGBBZ). Randomization was performed in the beginning of the project. Infants were randomly allocated to one of the following groups: blocked practice group (7 males, 5 girls), serial practice group (7 males, 5 girls), or control group (9 males, 3 girls) (Fig. 1). The researcher (first author) and infants’ parents were blind to the infants’ allocation to groups. A single physical therapist, who was another independent researcher (no co-author), unsealed the envelopes to know the infant’s allocation only after the baseline assessment, just before applying the practice or control protocols. The sequence in which the envelopes were opened, which defined each infant’s allocation, was the same as the sequence in which the infants had arrived at the laboratory for the baseline assessment. Infants were assessed at the onset of goal-directed reaching. To this end, infants’ parents were contacted by telephone, the details of which were provided by the maternity hospital of Sao Carlos. From two weeks before the infants’ three-month birthday, the researcher (first author) called the parents to inform them on the nature of the study and to invite them to participate. In order to establish the day of reaching onset, the researcher made home visits twice a week. During the visits, the infants were placed in a baby seat reclined at approximately 458 and the researcher presented an attractive toy at the infant’s midline and xiphoid process height, at his/her arm’s length (Fig. 2A). When infants were able to perform 3–5 reaches in approximately 1 min in a home visit, the assessment at the laboratory was scheduled to take place within the next five days (3.3  1.4 days). In the final home visit the examiner also applied the AIMS, a valid and reliable tool which assesses gross motor development of infants (Piper & Darrah, 1994). All infants were similar in their motor development at the period of reaching onset (percentile between 25 and 75 of the AIMS’s normative curve). Reliability value between two observers for AIMS scores computed for 14% of the sample was high (95.0%). Actual assessments were carried out at the laboratory 1–1.5 h after the infants’ feeding and care was taken that time and day did not coincide with nap periods or vaccination days. All infants were in diapers and were assessed three times: (1) immediately before the practice schedule (pre-test), (2) immediately after the practice schedule (post-test), and (3) approximately 24 h after post-test (retention). If the infant did not perform at least three reaches at the pre-test due to fuss, cry or inactivity, the assessments were rescheduled to occur within the next five days calculated from the final home visit. All infants were assessed under the same conditions. For the assessments, the markers were attached to the infant’ wrists (one marker to each wrist, between radius and ulna styloid processes). The markers were tightened such that they did not restrict the free movements of the wrists. The infant was placed in the baby chair and the researcher flattened one of her hands on the infant’s trunk to provide security and trunk

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Fig. 1. Study design.

Fig. 2. Assessment of reaching at home visits (A) and at the laboratory (B).

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stability. The toy was held by the researcher, who was positioned in front and out of the infant’s reaching distance. The toy was presented at the infant’s midline, at xiphoid process height, and at the arm’s length, for 2 min (Fig. 2B). During this period, the toy was carefully taken away and presented again to the infant after each successful toy contact (i.e., a reach). The interval between toy presentations was approximately 5 s. The toy was always oriented vertically along its major axis (Cunha, Soares, et al., 2013; Cunha, Woollacott, et al., 2013; Toledo et al., 2011). After the pre-test, the physical therapist opened the next sealed envelope and applied the practice protocols according to infants’ allocation. The physical therapist sat comfortably with her trunk supported, legs slightly apart, and hips and knees flexed, respectively, around 1208 and 508 (see figures in the Table 2). This position configured a similar arrangement as the chair used during the assessments (reclined 458, with back/headrest), minimizing body position effects between assessments and practice positions. A small pillow was placed on the physical therapist’s knees and the infant’s head was placed on the pillow. These procedures favored the infant to remain face to face with the physical therapist with his/her neck in semi-flexion, thus facilitating the alignment between the infant’s head and trunk and the position of hand near midline within his/her visual field. The blocked practice group received practice of stimulated reaching using the toy in three activities repeated under the basis of blocked schedule in both right (R) and L (left) arms [111(R)–111(L)–222(R)–222(L)– 333(R)–333(L); blocked practice group], whereas the serial practice group received practice of stimulated reaching using the toy in three activities repeated under the basis of serial schedule in both R and L arms [123(R)–123(L)–123(R)–123(L)– 123(R)–123(L); serial practice group]. Each activity was repeated six times in both groups; however, the groups differed in the order in which the activities were repeated (Table 2). Practice lasted approximately 4 min. The control group remained with the physical therapist at the same position as the practice groups engaged in verbal interaction during 4 min, but without receiving toy or reaching stimulation. These protocols were based on previous studies (Cunha, Soares, et al., 2013; Cunha, Woollacott, et al., 2013; Heathcock et al., 2008; Lobo, Galloway, & Savelsbergh, 2004; Soares, Cunha, Barbosa, Carvalho, & Tudella, 2010). All infants received experimental or control conditions as allocated. 2.4. Data analyses and dependent variables Movements of the hand toward the toy resulting in contact, regardless of grasping, were considered as reaching (Cunha, Soares, et al., 2013; Cunha, Woollacott, et al., 2013; Savelsbergh & van der Kamp, 1994; Toledo et al., 2011). The beginning of a reaching movement was defined as the first frame at which the infant started an uninterrupted movement of the hand toward the toy. The end of a reaching movement was designated as the first frame at which the infant’s hand touched the toy (Carvalho, Tudella, Caljouw, & Savelsbergh, 2008; Corbetta & Thelen, 1996; Cunha, Soares, et al., 2013; Cunha, Woollacott, et al., 2013). The primary outcome was reaching enhancement, measured by the difference in the number of reaches, in the proportions of proximal and distal adjustments and in the kinematic parameters of reaching between the pre- and post-tests and between the post-test and retention test. Grasping enhancement was the secondary outcome, measured by differences in the proportions of grasps. The number of reaches was computed as the total number of reaches performed during the 2 min assessments. Categorical variables included proximal and distal adjustments of reaching and grasping, and are described as follows: Proximal adjustments were categorized as follows: unimanual: the infant moved one hand toward the toy resulting in touching it (Corbetta & Thelen, 1996; Cunha, Soares, et al., 2013; Toledo et al., 2011); bimanual: the infant moved both hands simultaneously with a difference less than or equal to 20 frames for at least 50% of the trajectory toward the toy and touched it (Corbetta & Thelen, 1996; Cunha, Soares, et al., 2013; Rocha, Silva, & Tudella, 2006; Toledo et al., 2011). Distal adjustments were coded using the frame of the end of reaching movement and included hand opening: (a) open (the fingers were completely extended or slightly flexed), (b) closed (all fingers were completely flexed, or all fingers were completely flexed but one was extended [regardless of extension degree]), or (c) semi-open (the fingers were in an intermediate position in relation to the two aforementioned ones). Grasping outcome: (a) grasping (the infant grabbed the toy with his/her fingers using one or both hands after a valid reach) and (b) without-grasping (the infant reached the toy but did not grab it). Kinematic parameters comprised variables that characterize smoothness and velocity of reaching trajectory. The deceleration index indicates the proportion of time spent in decelerating the hand so that it touched the toy; it was calculated by the ratio between the time spent in the movement following the higher peak of velocity until the touch on the toy, and the total duration of the reaching movement, in percentage (Carvalho et al., 2007). The number of movement units consists of the number of acceleration and deceleration phases of the reaching trajectory and usually decreases with improved reaching control; it was defined as the number of maximum velocities between two minimum velocities, for which the difference was greater than 1 cm/s (Thelen, Corbetta, & Spencer, 1996; von Hofsten, 1979); the velocity was obtained by the vector norm (i.e., the square root of the addition of X, Y and Z squares). Mean velocity was obtained by calculating the ratio between the norm of the distance traveled by the hand and the duration of reaching (Mathew & Cook, 1990). In the case of bimanual reaches, only the hand that first touched the toy was analyzed. All variables were analyzed by one expert observer blind to the allocation of the infants to groups. For the coding reliability of the categorical variables (i.e., proximal and distal adjustments, and grasping), all reaches of 8 infants from the sample were analyzed independently by two experienced observers. The inter-observer reliability (agreement index) assessed by Cohen’s Kappa computed considering all categorical variables was found to be high (k = 0.98; 95% IC 0.01).

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The number of reaches was analyzed by counting the total number of reaches, and the categorical variables were analyzed by the proportions of their occurrence in relation to the number of reaches. The data was first analyzed on the basis of the tests of normality (Shapiro–Wilk) and homogeneity (Levene). The tests revealed that the categorical data were not normally distributed and transformations did not satisfy the normality assumption. Hence, the non-parametric Kruskal–Wallis test was used to compare groups (blocked practice, serial practice, control) at each assessment (pre-test, post-test, retention). When differences were significant, data were submitted to Mann–Whitney test for multiple comparisons with Bonferroni adjustments set at p < 0.017. To test differences between assessments, non-parametric repeated measures ANOVA (Friedman’s test) was used. The immediate effects of practice were tested comparing pre-test and post-test assessments in each group, whereas retention effects of practice were tested comparing post-test and retention assessments in each group. The kinematic variables were analyzed using mean values of reaches for each infant. The tests revealed that this data satisfied the normality and homogeneity assumptions and hence two-way mixed ANOVA was used to analyze effects of assessment (pre-test, post-test, retention) and group (blocked practice, serial practice, control) and interaction between these factors. For pre- and post-test comparisons, the statistics compared the original twelve infants per group. For post-test and retention comparisons, nine infants per group were compared because seven infants (two from each practice group and three from the control group) did not complete the retention test and, therefore, these seven infants plus one random infant from each practice group were excluded2 (i.e., resulting in three numerically homogeneous groups of nine infants) to allow for a direct comparison between groups. Effect sizes were calculated using r (r = Z-score/Htotal sample, where r  0.2: small effect; r > 0.2e  0.4: moderate effect; r  0.5: high effect) to non-parametric tests and Cohen’s d to parametric tests. 3. Results The late preterm infants from the blocked practice, serial practice and control groups started performing their first goaldirected reaches at 15.8  1.5, 16.2  0.7, 16.7  0.4 weeks of chronological age (p = 0.49), respectively. A total of 829 reaching movements were analyzed for the categorical variables: 244 at the pre-test, 347 at the post-test, and 238 at retention. For kinematics, reaching movements in which the marker was not picked up by one of the cameras or was not tracked automatically by the analysis system were excluded, hence a total of 402 reaches were analyzed: 134 reaches analyzed at the pre-test, 159 at the post-test, and 109 at the retention. 3.1. Number of reaches and categorical variables 3.1.1. Differences between groups There were no differences between groups in the number of reaches at the pre-test (X2 (2) = 1.72; p = 0.42; r’s < 0.25), the post-test (X2 (2) = 2.45; p = 0.29; r’s < 0.27) or at retention (X2 (2) = 0.12; p = 0.94; r’s < 0.07) (Fig. 3). The categorical variables were not affected by group either. 3.1.2. Immediate effects of practice Number of reaches. There was an increase in the number of reaches from the pre- to the post-test in the serial practice group (X2 (1) = 8.33; p < 0.01; r = 0.50) (Fig. 3). By contrast, there were no differences between pre- and post-test for the total number of reaches in either the blocked practice (X2 (1) = 0.33; p = 0.56; r = 0.18) or the control (X2 (1) = 2.27; p = 0.13; r = 0.25) groups. Proximal adjustments. The serial practice group increased the proportion of bimanual reaches from the pre- to the posttest (X2 (1) = 4.00; p < 0.05; r = 0.30) (Fig. 4). There were no differences between pre- and post-test for the proportions of bimanual reaches in either the blocked practice (X2 (1) = 1.18; p = 0.18; r = 0.11) or the control (X2 (1) = 3.00; p = 0.08; r = 0.27) groups. Distal adjustments and grasping outcome. From the pre- to the post-test, there were no differences for hand opening (X2’s (1) < 2.67; p’s > 0.10; r’s > 0.02) in any of the groups, but the proportions of grasping increased from the pre- to the post-test in the control group (X2 (1) = 6.00; p = 0.01; r = 0.37) (Fig. 5). There were no differences between pre- and post-test in either the blocked practice (X2 (1) = 0.67; p = 0.41; r = 0.12) or the serial practice (X2 (1) = 0.20; p = 0.65; r = 0.11) groups for the proportions of grasping. 3.1.3. Retention The results of retention will be reported only considering the variables that changed from pre- to post-test. Number of reaches. There was a decrease in the number of reaches from the post-test to the retention in the serial practice group (X2 (1) = 7.00; p = 0.01; r = 0.40) (Fig. 3). This indicates that the gain immediately after practice was not consolidated one day after. There were no differences for this variable between post-test and retention in either the blocked practice (X2 (1) = 2.78; p = 0.10) or the control (X2 (1) = 1.00; p = 0.32) groups.

2

Inclusion of these infants did not change the statistical outcomes, however.

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Fig. 3. Median number of reaches over assessments by groups (*p < 0.05). Error bars reflect confidence intervals.

Fig. 4. Median proportions of bimanual reaches over assessments by groups (*p < 0.05). Error bars reflect confidence intervals.

Fig. 5. Median proportions of reaches with grasping over assessments by groups (*p < 0.05). Error bars reflect confidence intervals.

Proximal adjustments. There were no differences between post-test and retention for the proportions of bimanual reaches in the serial practice group (X2 (1) = 0.00; p = 1.00; r = 0.06). Yet, numerically, the proportion of bimanual reaches decreased to pre-test level. There were no changes for this variable from the post-test to retention in either the blocked practice (X2 (1) = 0.00; p = 1.00) or the control (X2 (1) = 0.00; p = 1.00) groups (Fig. 4). Grasping outcome. There were no differences between the post-test and the retention for the proportions of grasping in the blocked practice (X2 (1) = 0.200; p < 0.655) and the serial practice (X2 (1) = 1.000; p < 0.317) groups. There were no changes for this variable from the post-test to retention in the control group (X2 (1) = 1.000; p < 0.317; r = 0.24), suggesting that the increase of this variable observed from pre- to post-test was retained (Fig. 5). 3.2. Kinematic variables There were no significant effects for the means of reaches in the kinematic variables. Data was submitted to Cohen’s test to evaluate the magnitude of effect. The observed effect size, however, were predominantly moderate to small (i.e., d < 0.3)

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Table 3 Statistical data of the ANOVA applied for the kinematic variables. Variables

Assessment effects

Group effects

Interaction

DI MU MV

F2,52 = 1.11; p = 0.34; d = 0.2 F2,52 = 0.46; p = 0.64; d = 0.1 F2,52 = 1.03; p = 0.36; d = 0.2

F2,26 = 0.58; p = 0.56; d = 0.2 F2,26 = 1.10; p = 0.35; d = 0.1 F2,26 = 0.88; p = 0.43; d = 0.3

F4,52 = 0.99; p = 0.42; d = 0.3 F4,52 = 0.10; p = 0.98; d = 0.1 F4,52 = 1.01; p = 0.41; d = 0.3

DI, deceleration index; MU, number of movement units; MV, mean velocity; d = Cohen’s d (effect size); d  0.2, small effect; d > 0.2e  0.5, moderate effect; d > 0.5, high effect.

Fig. 6. Median of deceleration index over assessments by groups. Error bars reflect confidence intervals. Different letters (a and b) reflect group differences (*p < 0.05).

(Table 3). Together with the lack of significance, this suggests that the reaching practice did not affect the kinematic parameters of reaching. As the pre-planned comparisons for the means of reaches in the kinematic variables did not show any differences, these variables were explored considering individual reaches. Due to the large variability and non-normality of data in this case, Kruskal–Wallis test and Friedman’s ANOVA were used to compare groups and assessments, respectively. The analysis indicated a group effect for deceleration index at post-test (X2 (2) = 8.151; p = 0.017). The blocked group presented lower deceleration index than the serial practice group (p = 0.009; r = 0.30). The blocked group also presented a lower, but nonsignificant deceleration index than the control group at the post-test (p = 0.029; r = 0.22; a = 0.017). In addition, there were differences between assessments for the blocked practice group (X2 (2) = 6.045, p = 0.049), characterized by decrease in the deceleration index from pre- to post-test (p = 0.008; r = 0.26) (Fig. 6). There were no differences for the number of movement units and mean velocity. 4. Discussion This study investigated the role of practice and contextual interference on the reaching behavior of late preterm infants at the onset of goal-directed reaching. We found an increase in the amount of reaches and bimanual reaches immediately after a short bout of reaching practice in a serial schedule compared to baseline. These changes were not retained one day later. First, it is important to highlight that the late preterm infants delayed the onset of reaching with two weeks to one month relative to full-term infants. That is, using an identical protocol Cunha, Soares, et al. (2013) reported the onset of reaching around 13 weeks of chronological age in full-term infants. This indicates that late preterm infants need more time to learn to perform their first reaches with spontaneous practice, despite they have had more time interacting with the environment being born prematurely. This suggests differences in early motor control between late pre-term infants and full-term infants. In fact, prematurity is associated with difficulties in cognitive and motor learning processes early in infancy, such as the acquisition and performance of foot kicking in the mobile paradigm at 3–5 months of age (Gekoski et al., 1984; Heathcock et al., 2004; Heathcock, Bhat, Lobo, Galloway, 2005). In addition, very preterm infants born with low birth weight show less consistent reaching behavior than full-term infants around the period of reaching onset (Heathcock et al., 2008). Even late preterm infants have less brain mass at birth compared to full-term infants (Adams-Chapman, 2006; Ricci et al., 2008) and are known to still perform different reaching strategies at 6 months corrected age (Toledo & Tudella, 2008; Toledo et al., 2011). The current study extends these findings by showing that potential limitations in the acquisition of goal-directed reaching are also present in late preterm infants and are already present at the onset of reaching. 4.1. Immediate effects of practice We hypothesized that late preterm infants who received few minutes of reaching practice would enhance their reaching behavior immediately after practice. We found that toy-oriented repetition of reaching movements for 4 min was indeed

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effective to promote increase in the total amount of reaches and in the amount of bimanual reaches immediately after practice, compared to baseline. This is in line with our first hypothesis and may suggest that late preterm infants are responsive to a very short bout of reaching practice when they have just started reaching. The short bout of additional experience may have increased the infants’ intrinsic motivation to reach as they were oriented to perceive and repeat successful hand contacts toward an attractive toy during practice. Reaching behavior results from the interactions between the infant’s motivation and his/her sensorimotor capabilities to perceive the object and to move in response to the task (Corbetta, Thelen, & Johnson, 2000). These interactions are linked to a history of previous perception-action experience (Gibson, 1986; Kamm, Thelen, & Jensen, 1990). Thus, in this study, the guided experience of perceiving and self-producing actions successfully at an age at which the infants start discovering a new way to act upon objects (i.e., reaching) may have temporarily facilitated perception-action matching and motivated the infants to perform more attempts. Thelen’s work showed that as infants become aroused, they may be more energetic and tend to move and kick more (Thelen & Smith, 1994; Thelen, Bradshaw, & Ward, 1981; Thelen, Fisher, Ridley-Johnson, & Griffin, 1982; Thelen, 1981). The late preterm infants, however, did not learn from the reaching practice in this study (i.e., no retention), suggesting that familiarity to the task during the experiment may have brought them in a better energetic state, thus arousing them to reach more, but insufficiently long to make more permanent changes in their reaching behavior. The temporarily increase in the amount of bimanual reaching after reaching practice may also have resulted from increased motivation to reach. According to Corbetta and Thelen (1996), effort and high energetic status of the upper limbs may arise synchronous coupling between the upper limbs in infants. Cunha, Soares, et al. (2013) found increased unimanual reaching immediately after 4 min of reaching practice, but late preterm infants in the present study may have struggled and consequently used bimanual reaches more often. Gro¨nqvist et al. (2011) suggested that the use of both hands symmetrically helped very preterm infants at 8 months corrected age to increase precision in a demanding task, that is, reaching for a moving object. In the present study, increased bimanual reaching might also have been an alternative strategy to suit their upper limb motor patterns to the increased amount of general reaches. This might reflect poor power control of arm muscles. 4.2. Effects of contextual interference We had expected that practice under blocked schedule regime, generally known to produce lower contextual interference in adults, would be more advantageous for enhancing reaching behavior. Surprisingly, however, the temporarily increase in the amount of reaching was found only in the serial practice group. This result might suggest that a late premature birth can have some influence on the infants’ ability to respond to a short bout of reaching practice. The practice protocol applied in the studies by Cunha, Soares, et al. (2013) and Cunha, Woollacott, et al. (2013), in which full-term infants were found to immediately enhance reaching (including more reaches with open hand and faster reaches) after 4 min of reaching practice, was similar to the blocked practice schedule of the present study. In the present study, however, blocked practice did not affect the late preterm infants and not even serial practice affected hand opening and mean velocity. Although we do not know if the full-term infants examined by Cunha, Soares, et al. (2013) and Cunha, Woollacott, et al. (2013) had consolidated the increased amount of reaching as there was no retention test, we do know that the late preterm infants of the current study did not succeed in retaining the increased amount of reaching after serial practice. Hence, the potential to benefit from a short bout of reaching practice at the onset of the skill may be diminished in late preterm infants compared to full-term infants at least for immediate effects. This possible disadvantage in benefiting from experience is reinforced by the delayed age of reaching onset in late preterm infants. Our results also suggest that the practice in a serial schedule might have configured a convenient organization of the practiced activities, being possibly more close to actual reaching and, therefore, suitable to the late preterm infants to respond to the serial practice with more reaches. However, we must be careful on concluding that this reflects a contextual interference effect because there were no clear treatment effects (group differences). Looking into the data in an exploratory way, surprisingly the blocked practice group spent less time decelerating the hand before contacting the toy after blocked practice compared to serial or no practice. It is interesting to compare these findings to the success in reaching for the toy after practice, which increased for the serial practice group but tended to decrease for the blocked practice group (see Fig. 2). Toledo and Tudella (2008) found that at 6 months corrected age, late preterm infants decelerated their hand more before touching the object than full-term infants apparently as a strategy to gain success in grasping. It might be that in the present study the infants reached more after the serial practice because they tended to decelerate their hand more strongly when reaching for the toy, while the opposite might be true for the blocked practice. As these observations are not fully reliable, this idea is necessarily speculative. Altogether these findings signal that contextual interference may have a potential effect on the ability of late preterm infants to respond to a short bout of reaching practice only and, therefore, it deserves further attention in studies that aim to investigate reaching practice in infants. 4.3. Retention The increments in reaching after serial practice were not retained, which refutes our hypothesis of more benefits from practice under lower than higher contextual interference at the onset of reaching. Hence, our results suggest that the

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reaching behavior of late preterm infants benefited only temporarily from a short bout of practice. There were no learning effects as a consequence of practice (i.e., no relatively permanent changes). Indeed, this study shows that changes in reaching behavior seem to be triggered after the first few minutes of experience in late preterm infants at the onset of reaching, but few minutes of experience are not sufficiently substantial to consolidate the changes for longer periods of time. This finding evidences the need for retention tests before drawing that learning occurs after short-term practice. Our results also indicate the need of longer, more intensive practice to consolidate the increments in reaching behavior in late preterm infants. In very preterm infants, Heathcock et al. (2008) found increased amount of reaches after four weeks of daily training of hand-toy interaction and reaching for 45 min compared to untrained very preterm infants. These changes improved over four additional weeks and also turned to be greater compared to untrained full-term infants at the eighth week of training, evidencing long-term effects at least in the scale of weeks. For the eighth week of training, the authors also reported that preterm infants contacted the toy with open hand more often than untrained preterm infants, which was not observed in the present study after a short bout of practice. Hence, longer-term effects in the amount of reaches and enhancement of the quality of reaching likely require more extended toy-oriented experience. The same is possibly true also for enhancement in reaching control, such as more smoothness and velocity of reaching, which were not affected by practice in this study. Strikingly, infants from the control group, which did not receive toy-oriented experience, increased the number of grasps at the post-test and retained it. It is first important to mention that by reaching onset, infants perform very primitive grasps, more known as primitive squeezes (Halverson, 1931), which in this study were characterized by the use of only some fingers to pick up the toy and then clumsily approach it to the chest or the mouth (Appendix – Video 1). The use of a malleable rubber toy in this study was probably a factor that favored such behavior. The verbal, face-to-face and smiling communications with the physical therapist may have stimulated more social interaction, but it is intriguing that this might have benefited the proportions of grasping without benefiting the amount of reaches. Future work could investigate further the role of a short bout of social interaction on reaching and grasping at reaching onset. 4.4. Clinical implications Late preterm infants are less mature physiologically and structurally than infants born at term age, and their neurodevelopmental outcomes often differ (Adams-Chapman, 2006; also see Engle, Tomashek, Wallman, & the Committee on Fetus and Newborn, 2007, for a review). This study reinforces such developmental differences by showing that late preterm infants seem to delay the age of onset of reaching and, therefore, that they might need additional experience to learn to perform successful goal-directed reaches with spontaneous practice (to ‘‘catch up’’). Late preterm newborns are also the fastest growing subgroup of neonates (Davidoff et al., 2006), accounting for three times higher healthcare costs than full-term infants in their first year of life due to adverse outcomes (McLaurin, Hall, Jackson, Owens, & Mahadevia, 2009). Literature has reported the importance of monitoring and providing late preterm infants with more specific and guided experiences interacting with toys as a tool to minimize possible developmental deviations (Dusing, Lobo, Lee, & Galloway, 2013; Soares, von Hofsten, & Tudella, 2012). Despite of this, late preterm infants usually do not qualify to early sensori-motor intervention programs due to their clinical similarity to full-term infants at birth (Dusing et al., 2013; Petrini et al., 2009). Hence, the reaching practice under the basis of serial schedule used in this study offers an alternative and easy tool to be applied by caregivers at home to provide late preterm infants with additional experience contacting toys. For example, Heathcock et al. (2008) has shown that daily practice of reaching applied by parents at home can advance and enhance reaching behavior in higher risk preterm infants. Although a short bout of practice is insufficient for consolidation of enhanced reaching behavior, therapists could adjust the current practice protocol regarding intensity, duration and toy to guide caregivers to apply it during dedicated play with their late preterm infants. We stress, however, that protocols must be tailored according to specific interventional aims and individual infants. This study also provides partial support to the immediate changes in the reaching behavior of preterm infants that therapists often experience in clinical practice after toy-oriented enticing, highlights the importance of each intervention session and reinforces the necessity of more intensive practice for longer-term effects. In addition, this study may be an initial step to empirically expand the practice protocols demonstrated here to other populations at biological risk for developmental delays, such as low-birth weight, very preterm infants, and infants with hand function limitations, such as those with cerebral palsy and obstetric brachial palsy.

5. Conclusions, limitations and future research This is the first study to show that at the onset of reaching, late preterm infants can respond to a very short bout of toyoriented reaching practice temporarily. Our major finding was that the late preterm infants immediately increased the amount of reaching after few minutes of reaching practice based on a serial schedule. Yet, the increase was not retained after 24 h. We suggest that the toy-oriented experience of perceiving and self-producing actions with success favored perceptionaction coupling and increased the infants’ motivation to perform more reaching attempts immediately after practice. Nevertheless, it was insufficiently long to bring about more lasting changes.

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It is important to stress that as we did not find differences between groups, this limits any interpretation regarding learning effects. More robust and long-term effects related to contextual interference in late preterm infants may come with more intensive practice. Future work should investigate changes in reaching behavior after practice across continuous and larger time periods. In addition, our sample may not be representative of general population of late preterm infants, including those from different cultures. The large individual variability in reaching behavior among the late preterm infants suggests that they differ substantially in the period of reaching onset. A larger sample could have improved the power to detect effects, if any. Thus, one must be careful before generalizing our findings to other populations. Moreover, we do not know whether apparent strategies, such as the use of bimanual reaching, are only transient. Although randomized controlled trials are known to provide evidence-based information for clinical practice primarily based on allocation of subjects of similar characteristics, comparing late preterm infants with full-term infants in future research can also shed more light on the effects observed in the present study. Further research could also verify if the increased amount of reaches and kinematic changes after a few minutes of toy-oriented practice in late preterm infants reflects the primary neural mechanisms that underlie motor reorganization just after movement repetition. Acknowledgements We kindly thank the caregivers and infants for the participation in this study. We thank Dr. Bruno Spolon Marangoni for performing the randomization and allocation concealment procedures. We also kindly thank Andre´a Baraldi Cunha, physical therapist and currently Doctorate student at the Federal University of Sao Carlos, Brazil, for applying the practice and control protocols in this study. We thank the support of research assistants from the Center of Studies in Neuropediatrics and Motricity (Nu´cleo de Estudos em Neuropediatria e Motricidade - NENEM), Federal University of Sa˜o Carlos, Brazil, during data collection and editing of the video files. We thank the Research Institute MOVE and the Faculty of Human Movement Sciences, VU University Amsterdam, The Netherlands, for accepting and supporting the first author in the institution during the preparation of this manuscript.

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The effect of a short bout of practice on reaching behavior in late preterm infants at the onset of reaching: a randomized controlled trial.

The purpose of this study was to examine the effects of a short bout of practice on reaching behavior in late preterm infants at the onset of goal-dir...
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