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Reaching skills of infants born very preterm predict neurodevelopment at 2.5 years
Infant Behavior and Development 57 (2019) 101333
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Reaching skills of infants born very preterm predict neurodevelopment at 2.5 years
T
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Ylva Fredriksson Kaula, , Kerstin Rosanderb, Helena Grönqvista, Katarina Strand Brodda,c, Lena Hellström-Westasa, Claes von Hofstenb a
Department of Women’s and Children’s Health, Uppsala University, Sweden Department of Psychology, Uppsala University, Sweden c Centre for Clinical Research Sörmland, Uppsala University, Sweden b
A R T IC LE I N F O
ABS TRA CT
Keywords: Cognition Language Motor function BSID-III Neurodevelopment
The purpose was to investigate associations between quality of reaching for moving objects at 8 months corrected age and neurodevelopment at 2.5 years in children born very preterm (gestational age (GA), 24–31 weeks). Thirtysix infants were assessed while reaching for moving objects. The movements were recorded by a 3D motion capture system. Reaching parameters included aiming, relative length of the reach, number of movement units, proportion of bimanual coupled reaches and number of hits. Neurodevelopment was assessed at 2.5 years by the Bayley Scales of Infant Development III. There were strong associations between infant reaching kinematics and neurodevelopment of cognition and language but the patterns differed: in children born extremely preterm (GA < 28 weeks), planning and control of reaching was strongly related to outcome, while in children born very preterm (GA 28–31 weeks) number of hits and bimanual strategies were of greater relevance. In conclusion, for extremely preterm infants, basic problems on how motion information is incorporated with action planning prevail, while in very preterm infants the coordination of bimanual reaches is more at the focus. We conclude that the results reflect GA related differences in neural vulnerability and that early motor coordination deficits have a cascading effect on neurodevelopment.
1. Introduction Reaching for objects is a foundation for infants’ ability to interact with and learn about the environment (Gibson, 1988; Gibson & Pick, 2000). It is the earliest observable goal directed action after gaze behavior and requires coordination of cognition and sensorimotor functioning. Reaching for moving objects also demands the ability to plan the action and predict the object’s motion. Already before the age of 5 months, typically developing infants aim ahead towards the future meeting point between the hand and
Abbreviations: BPD, bronchopulmonary dysplasia; BSID-III, Bayley Scales of Infant and Toddler Development, 3rd edition; CA, corrected age for prematurity; EPT, extremely preterm, i.e. born < 28 weeks of pregnancy; GA, gestational age; GW, gestational weeks; MU, movement unit; NEC, necrotizing enterocolitis; PDA, persistent ductus arteriosus; ROP, retinopathy of prematurity; SGA, small for gestational age; VPT, very preterm, i.e. born < 32 weeks of pregnancy ⁎ Corresponding author at: Uppsala University Hospital, 751 85 Uppsala, Sweden. E-mail addresses: [email protected] (Y.F. Kaul), [email protected] (K. Rosander), [email protected] (H. Grönqvist), [email protected] (K. Strand Brodd), [email protected] (L. Hellström-Westas), [email protected] (C. von Hofsten). https://doi.org/10.1016/j.infbeh.2019.101333 Received 2 December 2018; Received in revised form 13 May 2019; Accepted 9 June 2019 0163-6383/ © 2019 Elsevier Inc. All rights reserved.
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the moving object (von Hofsten, 2009). The neural underpinnings of reaching may be compromised in very preterm infants. Atkinson and Braddick (2011) hypothesized that a common underlying factor of this vulnerability can be traced to dorsal cortical processes that translate visual information into action control and that the vulnerability of this system is expressed differently depending on the degree of prematurity of the subject. Infants born very preterm, with gestational age (GA) less than 32 weeks, carry a risk of developing white matter damage to the visual afferent pathways in the neonatal period (Kostović & Judas, 2002) as well as later neurodevelopmental delay in motor, language and cognitive areas (Linsell, Malouf, Morris, Kurinczuk, & Marlow, 2015). Previous studies of reaching have consistently found that preterm birth is associated with poorer reaching kinematics compared to term birth (Lobo, Kokkini, Cuncha, & Galloway, 2015; Rönnqvist & Domellöf, 2006). Differences in movement organization persist at least until 8 years of age (Johansson, Domellöf, & Rönnqvist, 2014). We have previously demonstrated that infants born very preterm have poorer gaze tracking ability of a moving object than term infants (Brodd, Grönqvist, Holmström, Grönqvist, Rosander & Ewald, 2012; Grönqvist, Brodd, & Rosander, 2011). At 8 months corrected age (CA), infants born very preterm also use different reaching strategies, including more bimanual and circuitous approaches than term born peers when reaching for moving objects (Grönqvist, Brodd, & von Hofsten, 2011). Reaching for moving objects places special demands on cognitive, motor and motion perception functions to be successful. Reaching for stationary objects has been related to later neurodevelopment (Fallang, Saugstad, Grøgaard, & Hadders-Algra, 2003; Fallang, Øien, Hellem, Saugstad, & Hadders-Algra, 2005) and exploratory behavior at 6 months in very preterm children is associated with language and cognitive function at 24 months (Zuccarini, Guarnii, Iverson, Benassi, Savini, Alessandroni, et al., 2018). Also, tracing a trajectory of communication, several studies have found a relationship between early gesturing and pointing, and cuncurrent or later language function in children born extremely preterm (before week 27) or with very low birth weight (Benassi, Savini, Iverson, Guarini, Caselli, Alessandroni, et al., 2016; Sansavini, Guarini, Savini, Broccoli, Justice, Alessandroni, et al., 2011; Stolt, Mäkilä, Matomäki, Lehtonen, Lapinleimu & Haataja, 2014). Fallang and coworkers (Fallang et al., 2003, 2005) investigated the relationship between early reaching for stationary objects and later development in children born very preterm (GA 27–30 weeks). The results showed that poorer reaching kinematics at 4 months was related to lower scores on the Bayley Scales of Infant Development (BSID-II) psychomotor index but not to the mental developmental index, representing cognitive function, at 6 and 12 months CA. There was still a relationship between poorer reaching kinematics at 4 as well as at 6 months on one hand and lower fine motor ability and minor neurologic dysfunction at 6 years on the other (Fallang et al., 2005). Given the higher demands when reaching for moving objects compared to stationary ones, we hypothesized that the quality of reaching for a moving object would be more relevant in association with later neurodevelopment in children born very preterm. Thus, the purpose of the present study was to investigate the associations between quality of reaching for moving objects at 8 months and neurodevelopment at 2.5 years in children born very preterm. An increasing number of children are born preterm and studies are urgently needed to investigate intervention potentials and limitations. There is a lack of knowledge on how early interventions can be optimized. However, Zuccarini et al. (2018) suggested that preterm infants (GA < 27 weeks) at around 6 months CA would benefit from an intervention focused on exploratory handeling of suitable objects. Quality of reaching include kinematics related to visuomotor planning as well as execution of goal directed reaching. We tested the hypothesis that these kinematics predict neurodevelopmental performance at 2.5 years of age in very preterm infants. Also, we wanted to explore if being born extremely preterm (GA less than 28 weeks) or very preterm (GA 28–31 weeks) influenced possible associations.
2. Methods 2.1. Participants The 36 infants in the present study were part of a larger population based cohort of 109 very preterm infants born during a fouryear period (2004–2007) at Uppsala University hospital, Sweden, called the LOVIS-project (LOngitudinal multidisciplinary study of VISuomotor capacity in very preterm infants) involving the Departments of Women’s and Children’s Health, Psychology and Neuroscience at Uppsala University (Brodd et al., 2012). Inclusion criteria in the present study was absence of severe brain injury, defined as intraventricular hemorrhage grade 3–4 (IVH 3–4 or cystic periventricular leukomalacia (PVL), and participation in the reaching experiment and in the neurodevelopmental assessment at 2.5 years. Study results from the reaching experiment has been previously published (Grönqvist et al., 2011), and the study at hand constitutes a longitudinal follow up. Study group characteristics are reported in Table 1. For subgroup analyses the subjects were divided into two groups according to the degree of prematurity, extremely preterm (EPT) with GA less than 28 weeks, and very preterm (VPT) with GA 28–31 weeks (Table 1). Only one infant in the VPT group had experienced severe neonatal risk factors, i.e. ROP ≥ 3, BPD, or treated PDA (Grönqvist et al., 2011). Results were not influenced significantly by inclusion/removal of this single subject. The reaching assessment in the original study was conducted at a mean corrected age of 39 weeks and 5 days (interquartile range 35.4–39.2), that is, the mean age for this study is slightly higher than in the original sample of the reaching experiment (Grönqvist et al., 2011), because not all children participated in the BSID-III follow up. Age at reaching assessment for children born EPT did not differ from those born VPT (p = .57). Parental consent was obtained for clinical assessments and the reaching assessment separately. The study was approved by the Ethical Committee of the Medical faculty at Uppsala University (Ups 03-665) and was carried out in accordance with the declaration of Helsinki. 2
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Table 1 Study group characteristics, reaching parameters at 8 months and 2½-year outcome in the extremely and very preterm groups. Data are numbers or mean values (standard deviations) as indicated. P-values refers to difference between The very preterm and extremely preterm born groups. ** p < .01, * p < .05, n.s. not significant.
Perinatal data
Neonatal risk factors
Reaching parameters at 8 months CA
2.5-year outcome
Antenatal steroids Gestational age, weeks + days, mean (range) Birth weight, g Girls Small for gestational age Septicaemia Patent ductus arteriosus, treated Retinopathy of prematurity ≥3 Bronchopulmonary dysplasia Aiming, m(sd) Relative length, Movement units Number of hits Number of reaching attempts Number of bimanual hits Proportion of bimanual coupled reaches Number of bimanual coupled reaches Cerebral Palsy BSID-III Cognitive score Range BSID-III Receptive language score Range BSID-III Expressive language score Range BSID-III Fine motor score Range BSID-III Gross motor score Range
Preterm infants, n = 36
Extremely preterm infants, n = 13
Very preterm infants, n = 23
p-value
29 28.4 (24.6–31.9)
11 25.9 (24.6–27.9)
18 29.9 (28.0–31.9)
n.s. p < .01
1168 (306) 19 7 7 7 2 7 −1.5 (5.6)
912 (179) 7 2 5 5 2 6 −2.5 (6.1)
1312 (266) 12 5 2 2 0 1 −1 (5)
p< n.s. p< p< p< n.s. p< n.s
1.5 (0.3) 2.3 (0.6) 4.7 (4) 11.4 (6.2) 1.4 (1.8) 0.1 (0.1)
1.5 (0.3) 2.2 (0.7) 4.5(4.5) 12.1(5.1) 1.7(2.1) 0.15(0.13)
1.5 (0.3) 2.5 (0.6) 5.1 (3.9) 11.1 (6.8) 1.3 (1.7) 0.1 (0.1)
n.s. n.s. n.s. n.s. n.s. n.s.
1.5 (1.8) 1 10.8 (2.2) 8–16 11.2 (2.3) 6–16 12 (2.9) 6–19 12 (3) 6–18 8.2 (2.8) 1–13
2.3 (2.1) 0 10.5 (2.3) 8–15 10.8 (3) 6–16 11.5 (2.9) 7–15 11.7 (3.8) 6–18 7.5 (2.5) 4–12
1.2 (1.6) 1 11 (2.2) 8–16 11.5 (1.9) 8–15 12.3 (3) 6–19 12.2 (2.4) 7–18 8.6 (2.9) 1–13
n.s n.s. n.s.
.01 .05 .05 .05 .01
n.s. n.s. n.s. n.s.
2.2. Protocol Perinatal data were prospectively collected during the neonatal period (Brodd et al., 2012). The reaching assessments were conducted at the Baby Lab, Department of Psychology, Uppsala University. A special infant chair was used for supporting the hips and lower trunk of the infant while leaving the upper part of the body and the arms free (Bumbo Ltd, Gauteng, South Africa). With a parent close behind, the infant was placed in front of a vertical screen, where a small toy (diagonal 4 cm) moved along a semicircular trajectory (radius 35 cm) with its lowest point in front and within reach (20 cm distance) of the infant. The starting point was randomly assigned either to the top right or top left of the trajectory, and the toy then moved with a sinusoidally modulated velocity with maximum velocity in front of the infant (24 cm/s). Two passive reflective markers were placed on each hand of the infant and one on the small toy. Five ProReflex cameras (Qualisys, Gothenburg, Sweden) were placed above and to the sides of the infant to capture the coordinates of the moving hands and toy at a recording frequency of 240 Hz (Fig. 1 Experimental set up). (Grönqvist et al., 2011). 2.3. Kinematic parameters Goal directed motor actions are planned in advance and corrected through visual control during the action. The planning of a reach is reflected in how close the aiming is relative to the goal (Fig. 2). The straightness, or relative length, of the movement is another aspect of planning. This measure refers to the ratio between the path (cm) that the hand actually travels towards the object, and the shortest possible path (cm) between start and goal. A reach is organized in terms of velocity pulses, called movement units (MU), each consisting of an acceleration and a deceleration phase (von Hofsten, 1991). Adults usually use one MU when implementing a reach, which means that the velocity of the hand increases at the beginning of the movement and decreases towards the end of it. Infants, however, typically build goal directed reaching movements in a series of MUs. The MU covering the largest part of the distance towards the object is most often positioned at the beginning of the reach with the subsequent MUs correcting for errors in the initial trajectory. Over the first year of life, infants use a decreasing number of MUs, indicating more mature planning and execution of the reach. As the transition between the MUs often coincides with change in direction of the reach, the number of MUs and the relative length of the reach are related. Other aspects of reaching quality is indicated by strategies used by the infant to obtain the goal, eagerness in trying to catch the object and successrates of grabbing it. 3
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Fig. 1. The infant is sitting in front of the screen with the moving object ready to reach out for it. Reflective markers are placed on both hands and on the object.
Fig. 2. Aiming measures how well the infant anticipate the future meeting point between the hand and the moving object. The object position as the reach starts is at position (a) and moves to position (b) as the reach ends. The angle formed by the position of the hand at the start (c) and the positions of the object at the start (a) and at the end (b) of the reach is called β, and the angle formed between the positions of the object (a) and hand (c) at the start and the hand at the end (d) of the reach is called α. For a perfect aim α-β should equal 0, and for a predictive reach the hand should arrive at the interception point ahead of the object, as indicated by a negative value.
A movement was defined as a reach when one or two hands started to move consistently towards the trajectory of the object for a distance of 7 cm or more. The infants reached for the object 14 times on average (range 2–28), the mean of which was used in the analysis. The experiment was terminated when the infant no longer showed an interest in the task. A bimanual coupled reach was defined when the two hands were coordinated in time, i.e. set out for the object less than .5 s from each other (Grönqvist, Brodd, von Hofsten, 2011). All kinematic varables constitute mean values for the individual child, exept where specified as number or 4
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proportion. Detailed descriptions of the kinematic reaching parameters at 8 months were published previously (Grönqvist, Brodd, von Hofsten, 2011). Thus, the variables aiming and relative length, which are related to planning, and MUs, which are an expression of visuomotor control, will be referred to as visuomotor planning. Reach execution will referre to strategies (unimanual or bimanual, proportion of bimanually coupled reaches, number of hits and attempts) and how successful the infant was at grasping the object. 2.4. Assessment of preschool neurodevelopment The children were tested with the BSID-III (Bayley, 2006) at around 2.5 years CA (mean 32 months, range 28–41) by a licensed psychologist at the Department of Paediatrics, Uppsala University Hospital. The psychologist was blinded to the reaching assessment results. Due to the need for calculating CA to administer the BSID-III correctly, it was not possible to be blinded to GA. The BSID-III provides estimates on five subscales: cognition, receptive and expressive language, and fine and gross motor function. 2.5. Statistical procedures Data were compiled in IBM SPSS Statistics for Windows, Version 22.0 (Armonk, NY: IBM Corp. USA), with regression analysis performed separetly in R (open sorce). For comparisons between the EPT and VPT groups, Student’s t-test or Fishers’ exact test were used for parametric and non- parametric data respectively. As the proportion of infants with specific neonatal complications was low, controlling for each of them separately was considered unfeasible. Tests of normal distribution were carried out with Shapiro-Wilk’s test. Because of heteroscedasticity, only some of the BSID-III sub scales met the criteria for parametric testing (Shapiro Wilkes, pvalues ranging between .002 and .66), and for the sake of uniformity, Spearman correlations were performed to test all associations between reaching parameters and BSID-III results. Non parametric analysis could not address the question about interaction effects, how BSID-III results were dependent on reaching parameters. After statistical advice we performed linear regression models, with the reservation that the data did not meet criteria for parametric testing and that the sample size was not sufficient for the number of predictors required. To compensate for the heteroscedasticity, robust confidence intervals and p-values were computed using the Bell-McCaffrey robust standard errors (Imbens & Kolesar, 2016) as implemented in the R package clubSandwich. The predictors included in the analysis were grouping by gestational age (EPT, VPT), aiming and its interaction with gestational age groupning, as well as proportion of bimanual coupled reaches and its interaction with gestational age grouping. The focus of the analysises were on the interaction terms, and five models were performed – one for each BSID-III subscale. The variables of aiming and proportion of bimanual coupled reaches were selected because of their complexity and cognitive demands. Also, proportion of bimanual coupled reaches was the parameter that had differed between the preterm infants in the cohort compared to full term controls (Grönqvist, Brodd, von Hofsten, 2011). 3. Results Data for visuomotor planning and reach execution, are shown in Table 1 as well as group values for the BSID-III results. As observed in Table 1, the infants in the EPT group had more neonatal clinical risk factors than the VPT born infants. However, comparisons of reaching parameters between the EPT and VPT groups, revealed no statistical differences (p-values ranging between .10 and .99). Moreover, the overall BSID-III subscores did not differ significantly between the EPT and VPT children (Table 1). The mean scores for cognition, receptive and expressive language, and fine motor function, respectively, were all within +/- 1 SD of the Swedish published reference values. The scores for gross motor function did not differ statistically between the two groups in this sample but for the EPT group they were clearly below Swedish reference data (Månsson & Stjernqvist, 2014). In comparison to the reference data, 16 children had at least one BSID result < -1 SD, and eight had two or more < -1 SD. Four children had at least one result < -2 SD. Table 2 Spearman’s correlations co-efficient (r) values for reaching parameters at 8 months corrected age and Bayley Scales of Infant and Toddler Development (BSID III) subscale scores as assessed at 2.5 years of corrected age in children born preterm. Only statistically significant results are depicted. ** p < .01, * p < .05, † p < .06. For definitions of kinematic parameters, please see section 2.3.
Visuomotor planning Aiming Relative length Movement units Reach execution Number of bimanual reaching attempts Proportion of bimanual reaching attempts Number of bimanual coupled reaches Proportion of bimanual coupled reaches Number of reaching attempts Number of failed reaching attempts
Cognition
Receptive language
−.39* .48**
−.44** .34*
Expressive language
Fine motor
Gross motor
.42* .33†
.37* .35* .33* .43** .36*
.39* .36*
.32† .31† .35*
.36* .36*
.36*
5
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Table 3 Spearman´s correlations co-efficient (r) values for reaching parameters at 8 months corrected age and Bayley Scales of Infant and Toddler Development (BSID-III) subscale scores as assessed at 2.5 years of corrected age in children born extremely preterm (gestational age < 28 weeks) and very preterm (gestational age 28–31 weeks). Only statistically significant results are depicted. **p < .01, *p < .05, † p < .06. EPT, n = 13
Visuomotor Planning Aiming Relative length Movement units Reach execution Number of hits Number of reaching attmepts Number of bimanual hits Proportion of bimanual coupled reaches Number of bimanual coupled reaches
VPT, n = 23
Cognition
Receptive Language
Expressive Language
−.77** .74** .68*
−.65* .64* .55*
−.62* .71** .58*
Fine Motor
Gross Motor
Cognition
Receptive Language
Expressive Language
Fine motor
Gross Motor
−.50*
.52* .40†
.54**
.42*
.51* .65**
.43*
.61**
.43*
.41†
For the whole group of children, several reaching parameters at 8 months were related to neurodevelopment at 2.5 years, especially for cognition and the receptive language subscale (Table 2). A better visuomotor planning and reach execution related to higher cognitive and language subscale scores. The parameters that showed the highest correlations were relative length, aiming, and the proportion of bimanual coupled reaches. Fewer associations were found for reaching parameters and fine- and gross motor scores (Table 2). For the reach execution parameters (number of attempts, bimanual reaches, and coupled reaches as well as proportion of bimanual coupled reaches), all significant associations were positive indicating that the more attempts to obtain the object, the more bimanual strategies were used and the higher the success rate – the better the neurodevelopmental outcome. In addition, the regression models indicate interaction effects for aiming and gestational age grouping, for cognition (p = .056) and for expressive language (p = .095) although not reaching statistical significance. When split into sub groups according to gestational age, the patterns of associations between reaching parameter and BSID subscales differed between EPT and VPT infants (Table 3). Importantly, reaching data variance was similar in the two groups. In the EPT group, aiming, relative length, and number of MUs correlated significantly with BSID scores for cognition and language. In the VPT group, the total number of attempts, coupled reaches, hits and bimanual hits were associated with cognition, and receptive and expressive language.In the VPT group, there were also correlations between aiming and BSID fine motor function scores, and between number of hits and BSID gross motor scores. Within the EPT group, the number of MUs correlated with aiming (r = .56, p = .03) and relative length (r = .86, p < .001). In the VPT group, relative length and number of MUs and relative length were interrelated (r = .63, p < .001) but neither of these parameters were related to aiming. 4. Discussion Aspects of visuomotor planning and control, as well as of reach execution were both connected to outcome. Kinnematics relevant to planning the reach in advance, such as aiming and relative length were related to cognitive, language and fine motor outcome. The use of both hands in coordination was related to several of the later outcome measures. This was more important than how often the infant succeeded in catching the object. Successful reaching gives the infant an opportunity for exploration, which has been shown to give a cascading effect on later academic achievement in typically developing children (Bornstein, Hahn, & Suwalsky, 2013). The relationship has been confirmed in children born extremely preterm (< 28 GW) children up to two years of age (Zuccarini et al., 2017). Importantly, the relationship between early reaching and later neurodevelopment differed between EPT and VPT infants. In EPT infants, the visuomotor planning and control of reaching correlated strongly with later cognition and language scores at 2.5 years. In contrast, the relationship between reaching and neurodevelopment in the VPT children was reflected in the executional aspects of reaching. In addition, indications of interaction effects between aiming and gestational age grouping on cognition and expressive language suggest that cognitive and expressive language scores was not affected by aiming for the VPT group but for the EPT group higher cognitive and expressive laguage score was indicated by a more predictive aim. Somewhat surprisingly, the results suggest that the EPT infants with more MUs and a more circuitous reaching trajectory, also aimed their reaches further ahead of the moving object and had higher scores on the neurodevelopmental assessment. Being ahead of the object is a better strategy for a successful reach than lagging behind because it allows slowing down of the hand to meet the object. In contrast, a lagging reach necessitates speeding up and chasing the object. In other words, being ahead is advantageous 6
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because it gives extra time for zooming in on the object, giving rise to more MUs. However, this strategy may also be associated with later motor problems, which could explain the abscence of associations to later motor results on the BSID-III. Subjects who are motorically disadvantaged are expected to have a more circuitous reaching trajectory and have more MUs to compensate for this. Forsström and von Hofsten (1982) found that children with neurological impairments consistently aimed their reaches more ahead of the object as compared to typically developing children, and the relative lengths of their reaches were larger. In the LOVIS cohort, the infants who had a more pronounced neuromotor deficit at 10 months, aimed further ahead than infants with better neuromotor function (Grönqvist, Brodd, von Hofsten, 2011). A previous comparison of the very preterm infants with full term infants in Grönqvist, Brodd, von Hofsten (2011) showed that both groups were on average equally successful in catching a moving object, but the preterm infants used more bimanual reaches. The present results suggest advantages for the preterm infants with more bimanual reaching. The suggested relationships between individual reaching parameters and neurodevelopment may in part be due to differences in motor development that prevail during the first year of life in infants born EPT as compared to those who are VPT and/or without neonatal complications (Montgomery, Hellström-Westas, Strand Brodd, Sonnander, & Persson, 2017). Schneider et al. (2008) found an impairment in programming of visuomotor uni- and bi-manual tasks at 8 years for children born EPT, but not for children born at later gestational ages. The present results show that early visuomotor skills in infants born very preterm are closely related to later cognitive abilities. These findings are in agreement with Kaul, Rosander, von Hofsten, Brodd, Holmström, Kaul, et al., 2016 who demonstrated that gaze tracking at 4 months CA is related to neurodevelopment at 2.5 years of age. As hypothesized, reaching for moving objects showed a stronger relationship to later cognitive development than studies of reaching for stationary objects (Fallang et al., 2003, Fallang et al., 2005). Another study comparing reaching for moving objects in preterm and full term infants (van der Meer, van der Weel, Lee, Laing, & Lin, 1995) found a delay in onset of reaching and in choice of most effective strategy for the preterm group. The infants who had not switched to the more effective strategy at 48 weeks were later diagnosed with CP. The authors conclude, that a catching task could be useful in detecting brain damage. To catch a moving object, we rely on internal models of events that have not yet occurred. This process has similarities with expressive language (Ellis, Robledo Gonzalez, & Deák, 2014). In addition, a connection between early motor function and later communicative skills has been demonstrated in extremely preterm infants (Benassi et al., 2016). Also, parental ratings and observational studies of gestures, pointing and object manipulation in children born preterm further support to the idea that through early motor development the infant gets new opportunities to refine skills that are shared between numeous functions, including language (Iverson, 2010). It is argued that several constraints are posed by prematurity on the development of the infant, where alterations in motor, perceptual and communicative functions limits the typical development of language (Sansavini et al., 2011; Stolt et al., 2014; Zuccarini et al., 2018). A recent study by Gottwald, Achermann, Marciszko, Lindskog, and Gredebäck (2016) established the relation between kinematics of reaching and executive functioning in a group of healthy 18 month-old toddlers. The velocity peak of the first MU was related to inhibition and working memory on concurrent tasks. Our results connect reaching parameters at 8 months to neurodevelopment at later ages, further supporting the idea that reaching could be an early executive function marker and that motor control and executive function early in life could share a common base. In line with a number of experimental studies on visuomotor processing in premature infants (Atkinson & Braddick, 2011) the present data are interpreted according to dorsal stream vulnerability. They (Atkinson & Braddick, 2007; Braddick, Atkinson, & Wattam-Bell, 2011) found evidence that impairments of the dorsal visual pathways in infants born preterm are associated with an increased risk of motor disturbance and cognitive deficits. Taken together, our data (Table 3) indicate that the development of visual control of reaching in EPT and VPT follow different patterns. The indication is that in EPT children, basic motion perception and prediction of action goals are affected and in VPT children the coordination of bimanual actions. Bimanual reaching reflects a different aspect of the dorsal process than the planning itself. It is about coordinated sequences in time that goes beyond simple transformation of visuospatial information, and has been found to be sensitive to white matter damage (Birtles, Anker, Atkinson, Shellens, Briscoe, Mahoney, et al., 2011). Most mean BSID-III results for both the EPT and the VPT children are within +- 1 SD of the age equivalent EXPRESS study control group (Månsson & Stjernqvist, 2014) and when EPT and VPT groups of the present study are compared, no average differences between the kinematic data or BSID results are found. It is remarkable that the BSID-III results are so good on the average in both groups. The selection of the participants excluding severe braindamage or the inherent properties of the BSID-III, may in part explain this finding. It should also be noted, that neonatal riskfactors are more common within the EPT group. For understanding the developmental impact of extreme prematurity the infants abilities should be measured at two or more occasions as meassurments are similar between groups at both assessment points, but in relations between the two differences appear. The present study indicate that if the EPT infants are less matured than the VPT at 8 months the difference persists at 2.5 years. 5. Conclusion The different associations between reaching parameters and neurodevelopment indicate that several maturational processes may be involved in early reaching influence neurodevelopment. For the control of reaching for moving objects in the EPT children, more basic problems prevail that depend on how motion information is incorporated with action planning. For the VPT children, coordination of bimanual coupled reaches is more at the focus. The findings may be used for differentiating interventions with respect to GA. 7
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Funding Financial support was obtained from the Queen Silvia´s Jubilee Foundation, Stockholm, Sweden; the Linnéa and Josef Carlsson Foundation, Helsingborg, Sweden; the Jerring Foundation, Stockholm, Sweden; the Gillbergska Foundation, Uppsala, Sweden and the Swedish Research Council (2009-1093) and (2016-03109). None of the funders have in any way been involved in any step of the study. Acknowledgements We thank all children and parents who participated in the study. We also acknowledge the work by the following: professor Uwe Ewald, associate professor Bo Strömberg, professor Gerd Holmström, associate professor Pär Nyström, associate professor Olga Kochukhova, psychologist Ingela Helling. Special thanks to Lars Lindhagen for statistical consultations. References Atkinson, J., & Braddick, O. (2007). Visual and visuocognitive development in children born very prematurely. Progress in Brain Research, 164, 123–149. https://doi. org/10.1016/S0079-6123(07)64007-2. Atkinson, J., & Braddick, O. (2011). From genes to brain development to phenotypic behavior: "Dorsal-stream vulnerability" in relation to spatial cognition, attention, and planning of actions in Williams Syndrome (WS) and other developmental disorders. Progress in Brain Research, 189, 261–283. https://doi.org/10.1016/B9780-444-53884-0.00029-4. Bayley, N. (2006). Bayley scales of infant and toddler development (3rd ed.). San Antonio, TX: Harcourt Assessment. Benassi, E., Savini, S., Iverson, J. M., Guarini, A., Caselli, M. C., Alessandroni, R., et al. (2016). Early communicative behaviors and their relationship to motor skills in extremely preterm infants. Research in Developmental Disabilities, 48, 132–144. https://doi.org/10.1016/j.ridd.2015.10.017. Birtles, D., Anker, S., Atkinson, J., Shellens, R., Briscoe, A., Mahoney, M., et al. (2011). Bimanual strategies for object retrieval in infants and young children. 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J., & Pick, A. (2000). An ecological approach to perceptual learning and development. Oxford: Oxford University Press. Gottwald, J. M., Achermann, S., Marciszko, C., Lindskog, M., & Gredebäck, G. (2016). An embodied account of early executive-function development. Psychological Science, 27(12), 1600–1610. https://doi.org/10.1177/0956797616667447. Grönqvist, H., Brodd, K. S., & Rosander, K. (2011). Development of smooth pursuit eye movements in very prematurely born infants: 2. The low-risk subgroup. Acta Paediatrica, 100(7), e5–11. https://doi.org/10.1111/j.1651-2227.2011.02247.x. Grönqvist, H., Brodd, K. S., & von Hofsten, C. (2011). Reaching strategies of very preterm infants at 8 months corrected age. Experimental Brain Research, 209(2), 225–233. https://doi.org/10.1007/s00221-011-2538-x. Imbens, G. W., & Kolesar, M. (2016). Robust standard errors in small samples: Some practical advice. Review of Economics and Statistics, 98(4), 701–712. https://doi. org/10.1162/REST_a_00552. Iverson, J. M. (2010). Developing language in a developing body: The relationship between motor development and language development. Journal of Child Language, 37(2), 229–261. https://doi.org/10.1017/S0305000909990432. Johansson, A. M., Domellöf, E., & Rönnqvist, L. (2014). Long-term influences of a preterm birth on movement organization and side specialization in children at 4–8 years of age. Developmental Psychobiology, 56(6), 1263–1277. https://doi.org/10.1002/dev.21206. Kaul, Y. F., Rosander, K., von Hofsten, C., Brodd, K. S., Holmström, G., Kaul, A., et al. (2016). Visual tracking in very preterm infants at 4 mo predicts neurodevelopment at 3 y of age. Pediatric Research, 80(1), 35–42. https://doi.org/10.1038/pr.2016.37. Kostović, I., & Judas, M. (2002). Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anatomical Record, 267(1), 1–6. https://doi.org/10.1002/ar.10069. Linsell, L., Malouf, R., Morris, J., Kurinczuk, J. J., & Marlow, N. (2015). Prognostic factors for poor cognitive development in children born very preterm or with very low birth weight: A systematic review. JAMA Pediatrics, 169(12), 1162–1172. https://doi.org/10.1001/jamapediatrics.2015.2175. Lobo, M. A., Kokkini, E., Cuncha, A. B., & Galloway, J. C. (2015). Infants born preterm demonstrate impaired object exploration behaviors throughout infancy and toddlerhood. Physical Therapy, 95(1), 51–64. https://doi.org/10.2522/ptj.20130584. Månsson, J., & Stjernqvist, K. (2014). Children born extremely preterm show significant lower cognitive, language and motor function levels compared with children born at term, as measured by the Bayley-III at 2.5 years. Acta Paediatrica, 103(May (5)), 504–511. https://doi.org/10.1111/apa.12585. Montgomery, C., Hellström-Westas, L., Strand Brodd, K., Sonnander, K., & Persson, K. (2017). The structured observation of motor performance in infants has convergent and discriminant validity in preterm and term infants. Acta Paediatrica, 106(May (5)), 740–748. https://doi.org/10.1111/apa.13774. Rönnqvist, L., & Domellöf, E. (2006). Quantitative assessment of right and left reaching movements in infants: A longitudinal study from 6 to 36 months. Developmental Psychobiology, 48(6), 444–459. https://doi.org/10.1002/dev.20160. Sansavini, A., Guarini, A., Savini, S., Broccoli, S., Justice, L., Alessandroni, R., et al. (2011). Longitudinal trajectories of gestural and linguistic abilities in very preterm infants in the second year of life. Neuropsychologia, 49, 3677–3688. Schneider, C., Nadeau, L., Bard, C., Lambert, J., Majnemer, A., Malouin, F., et al. (2008). Visuo-motor coordination in 8-year-old children born pre-term before and after 28 weeks of gestation. Developmental Neurorehabilitation, 11(3), 215–224. https://doi.org/10.1080/17518420801887547. Stolt, S., Mäkilä,̈ A.-M., Matomaäki, J., Lehtonen, L., Lapinleimu, H., & Haataja, L. (2014). The development and predictive value of gestures in very-low- birth-weight children: A longitudinal study. International Journal of Speech-Language Pathology, 16(2), 121–131. https://doi.org/10.3109/17549507.2013.794861. van der Meer, A. L., van der Weel, F. R., Lee, D. N., Laing, I. A., & Lin, J. P. (1995). Development of prospective control of catching moving objects in preterm at-risk infants. Developmental Medicine & Child Neurology, 37(2), 145–158. von Hofsten, C. (1991). Structuring of early reaching movements: A longitudinal study. Journal of Motor Behavior, 23(4), 280–292. https://doi.org/10.1080/
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00222895.1991.9942039. von Hofsten, C. (2009). Action, the foundation for cognitive development. Scandinavian Journal of Psychology, 50(6), 617–623. https://doi.org/10.1111/j.1467-9450. 2009.00780.x. Zuccarini, M., Guarini, A., Savini, S., Iverson, J. M., Aureli, T., Alessandroni, R., et al. (2017). Object exploration in extremely preterm infants between 6 and 9 months and relation to cognitive and language development at 24 months. Research in Developmental Disabilities, 68, 140–152. https://doi.org/10.1016/j.ridd.2017.06. 002. Zuccarini, M., Guarini, A., Iverson, J. M., Benassi, E., Savini, S., Alessandroni, R., et al. (2018). Does early object exploration support gesture and language development in extremely preterm infants and full-term infants? Journal of Communication Disorders, 76, 91–100. https://doi.org/10.1016/j.jcomdis.2018.09.004.
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Infant Behavior and Development journal homepage: www.elsevier.com/locate/inbede
Full length article
Reaching skills of infants born very preterm predict neurodevelopment at 2.5 years
T
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Ylva Fredriksson Kaula, , Kerstin Rosanderb, Helena Grönqvista, Katarina Strand Brodda,c, Lena Hellström-Westasa, Claes von Hofstenb a
Department of Women’s and Children’s Health, Uppsala University, Sweden Department of Psychology, Uppsala University, Sweden c Centre for Clinical Research Sörmland, Uppsala University, Sweden b
A R T IC LE I N F O
ABS TRA CT
Keywords: Cognition Language Motor function BSID-III Neurodevelopment
The purpose was to investigate associations between quality of reaching for moving objects at 8 months corrected age and neurodevelopment at 2.5 years in children born very preterm (gestational age (GA), 24–31 weeks). Thirtysix infants were assessed while reaching for moving objects. The movements were recorded by a 3D motion capture system. Reaching parameters included aiming, relative length of the reach, number of movement units, proportion of bimanual coupled reaches and number of hits. Neurodevelopment was assessed at 2.5 years by the Bayley Scales of Infant Development III. There were strong associations between infant reaching kinematics and neurodevelopment of cognition and language but the patterns differed: in children born extremely preterm (GA < 28 weeks), planning and control of reaching was strongly related to outcome, while in children born very preterm (GA 28–31 weeks) number of hits and bimanual strategies were of greater relevance. In conclusion, for extremely preterm infants, basic problems on how motion information is incorporated with action planning prevail, while in very preterm infants the coordination of bimanual reaches is more at the focus. We conclude that the results reflect GA related differences in neural vulnerability and that early motor coordination deficits have a cascading effect on neurodevelopment.
1. Introduction Reaching for objects is a foundation for infants’ ability to interact with and learn about the environment (Gibson, 1988; Gibson & Pick, 2000). It is the earliest observable goal directed action after gaze behavior and requires coordination of cognition and sensorimotor functioning. Reaching for moving objects also demands the ability to plan the action and predict the object’s motion. Already before the age of 5 months, typically developing infants aim ahead towards the future meeting point between the hand and
Abbreviations: BPD, bronchopulmonary dysplasia; BSID-III, Bayley Scales of Infant and Toddler Development, 3rd edition; CA, corrected age for prematurity; EPT, extremely preterm, i.e. born < 28 weeks of pregnancy; GA, gestational age; GW, gestational weeks; MU, movement unit; NEC, necrotizing enterocolitis; PDA, persistent ductus arteriosus; ROP, retinopathy of prematurity; SGA, small for gestational age; VPT, very preterm, i.e. born < 32 weeks of pregnancy ⁎ Corresponding author at: Uppsala University Hospital, 751 85 Uppsala, Sweden. E-mail addresses: [email protected] (Y.F. Kaul), [email protected] (K. Rosander), [email protected] (H. Grönqvist), [email protected] (K. Strand Brodd), [email protected] (L. Hellström-Westas), [email protected] (C. von Hofsten). https://doi.org/10.1016/j.infbeh.2019.101333 Received 2 December 2018; Received in revised form 13 May 2019; Accepted 9 June 2019 0163-6383/ © 2019 Elsevier Inc. All rights reserved.
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the moving object (von Hofsten, 2009). The neural underpinnings of reaching may be compromised in very preterm infants. Atkinson and Braddick (2011) hypothesized that a common underlying factor of this vulnerability can be traced to dorsal cortical processes that translate visual information into action control and that the vulnerability of this system is expressed differently depending on the degree of prematurity of the subject. Infants born very preterm, with gestational age (GA) less than 32 weeks, carry a risk of developing white matter damage to the visual afferent pathways in the neonatal period (Kostović & Judas, 2002) as well as later neurodevelopmental delay in motor, language and cognitive areas (Linsell, Malouf, Morris, Kurinczuk, & Marlow, 2015). Previous studies of reaching have consistently found that preterm birth is associated with poorer reaching kinematics compared to term birth (Lobo, Kokkini, Cuncha, & Galloway, 2015; Rönnqvist & Domellöf, 2006). Differences in movement organization persist at least until 8 years of age (Johansson, Domellöf, & Rönnqvist, 2014). We have previously demonstrated that infants born very preterm have poorer gaze tracking ability of a moving object than term infants (Brodd, Grönqvist, Holmström, Grönqvist, Rosander & Ewald, 2012; Grönqvist, Brodd, & Rosander, 2011). At 8 months corrected age (CA), infants born very preterm also use different reaching strategies, including more bimanual and circuitous approaches than term born peers when reaching for moving objects (Grönqvist, Brodd, & von Hofsten, 2011). Reaching for moving objects places special demands on cognitive, motor and motion perception functions to be successful. Reaching for stationary objects has been related to later neurodevelopment (Fallang, Saugstad, Grøgaard, & Hadders-Algra, 2003; Fallang, Øien, Hellem, Saugstad, & Hadders-Algra, 2005) and exploratory behavior at 6 months in very preterm children is associated with language and cognitive function at 24 months (Zuccarini, Guarnii, Iverson, Benassi, Savini, Alessandroni, et al., 2018). Also, tracing a trajectory of communication, several studies have found a relationship between early gesturing and pointing, and cuncurrent or later language function in children born extremely preterm (before week 27) or with very low birth weight (Benassi, Savini, Iverson, Guarini, Caselli, Alessandroni, et al., 2016; Sansavini, Guarini, Savini, Broccoli, Justice, Alessandroni, et al., 2011; Stolt, Mäkilä, Matomäki, Lehtonen, Lapinleimu & Haataja, 2014). Fallang and coworkers (Fallang et al., 2003, 2005) investigated the relationship between early reaching for stationary objects and later development in children born very preterm (GA 27–30 weeks). The results showed that poorer reaching kinematics at 4 months was related to lower scores on the Bayley Scales of Infant Development (BSID-II) psychomotor index but not to the mental developmental index, representing cognitive function, at 6 and 12 months CA. There was still a relationship between poorer reaching kinematics at 4 as well as at 6 months on one hand and lower fine motor ability and minor neurologic dysfunction at 6 years on the other (Fallang et al., 2005). Given the higher demands when reaching for moving objects compared to stationary ones, we hypothesized that the quality of reaching for a moving object would be more relevant in association with later neurodevelopment in children born very preterm. Thus, the purpose of the present study was to investigate the associations between quality of reaching for moving objects at 8 months and neurodevelopment at 2.5 years in children born very preterm. An increasing number of children are born preterm and studies are urgently needed to investigate intervention potentials and limitations. There is a lack of knowledge on how early interventions can be optimized. However, Zuccarini et al. (2018) suggested that preterm infants (GA < 27 weeks) at around 6 months CA would benefit from an intervention focused on exploratory handeling of suitable objects. Quality of reaching include kinematics related to visuomotor planning as well as execution of goal directed reaching. We tested the hypothesis that these kinematics predict neurodevelopmental performance at 2.5 years of age in very preterm infants. Also, we wanted to explore if being born extremely preterm (GA less than 28 weeks) or very preterm (GA 28–31 weeks) influenced possible associations.
2. Methods 2.1. Participants The 36 infants in the present study were part of a larger population based cohort of 109 very preterm infants born during a fouryear period (2004–2007) at Uppsala University hospital, Sweden, called the LOVIS-project (LOngitudinal multidisciplinary study of VISuomotor capacity in very preterm infants) involving the Departments of Women’s and Children’s Health, Psychology and Neuroscience at Uppsala University (Brodd et al., 2012). Inclusion criteria in the present study was absence of severe brain injury, defined as intraventricular hemorrhage grade 3–4 (IVH 3–4 or cystic periventricular leukomalacia (PVL), and participation in the reaching experiment and in the neurodevelopmental assessment at 2.5 years. Study results from the reaching experiment has been previously published (Grönqvist et al., 2011), and the study at hand constitutes a longitudinal follow up. Study group characteristics are reported in Table 1. For subgroup analyses the subjects were divided into two groups according to the degree of prematurity, extremely preterm (EPT) with GA less than 28 weeks, and very preterm (VPT) with GA 28–31 weeks (Table 1). Only one infant in the VPT group had experienced severe neonatal risk factors, i.e. ROP ≥ 3, BPD, or treated PDA (Grönqvist et al., 2011). Results were not influenced significantly by inclusion/removal of this single subject. The reaching assessment in the original study was conducted at a mean corrected age of 39 weeks and 5 days (interquartile range 35.4–39.2), that is, the mean age for this study is slightly higher than in the original sample of the reaching experiment (Grönqvist et al., 2011), because not all children participated in the BSID-III follow up. Age at reaching assessment for children born EPT did not differ from those born VPT (p = .57). Parental consent was obtained for clinical assessments and the reaching assessment separately. The study was approved by the Ethical Committee of the Medical faculty at Uppsala University (Ups 03-665) and was carried out in accordance with the declaration of Helsinki. 2
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Table 1 Study group characteristics, reaching parameters at 8 months and 2½-year outcome in the extremely and very preterm groups. Data are numbers or mean values (standard deviations) as indicated. P-values refers to difference between The very preterm and extremely preterm born groups. ** p < .01, * p < .05, n.s. not significant.
Perinatal data
Neonatal risk factors
Reaching parameters at 8 months CA
2.5-year outcome
Antenatal steroids Gestational age, weeks + days, mean (range) Birth weight, g Girls Small for gestational age Septicaemia Patent ductus arteriosus, treated Retinopathy of prematurity ≥3 Bronchopulmonary dysplasia Aiming, m(sd) Relative length, Movement units Number of hits Number of reaching attempts Number of bimanual hits Proportion of bimanual coupled reaches Number of bimanual coupled reaches Cerebral Palsy BSID-III Cognitive score Range BSID-III Receptive language score Range BSID-III Expressive language score Range BSID-III Fine motor score Range BSID-III Gross motor score Range
Preterm infants, n = 36
Extremely preterm infants, n = 13
Very preterm infants, n = 23
p-value
29 28.4 (24.6–31.9)
11 25.9 (24.6–27.9)
18 29.9 (28.0–31.9)
n.s. p < .01
1168 (306) 19 7 7 7 2 7 −1.5 (5.6)
912 (179) 7 2 5 5 2 6 −2.5 (6.1)
1312 (266) 12 5 2 2 0 1 −1 (5)
p< n.s. p< p< p< n.s. p< n.s
1.5 (0.3) 2.3 (0.6) 4.7 (4) 11.4 (6.2) 1.4 (1.8) 0.1 (0.1)
1.5 (0.3) 2.2 (0.7) 4.5(4.5) 12.1(5.1) 1.7(2.1) 0.15(0.13)
1.5 (0.3) 2.5 (0.6) 5.1 (3.9) 11.1 (6.8) 1.3 (1.7) 0.1 (0.1)
n.s. n.s. n.s. n.s. n.s. n.s.
1.5 (1.8) 1 10.8 (2.2) 8–16 11.2 (2.3) 6–16 12 (2.9) 6–19 12 (3) 6–18 8.2 (2.8) 1–13
2.3 (2.1) 0 10.5 (2.3) 8–15 10.8 (3) 6–16 11.5 (2.9) 7–15 11.7 (3.8) 6–18 7.5 (2.5) 4–12
1.2 (1.6) 1 11 (2.2) 8–16 11.5 (1.9) 8–15 12.3 (3) 6–19 12.2 (2.4) 7–18 8.6 (2.9) 1–13
n.s n.s. n.s.
.01 .05 .05 .05 .01
n.s. n.s. n.s. n.s.
2.2. Protocol Perinatal data were prospectively collected during the neonatal period (Brodd et al., 2012). The reaching assessments were conducted at the Baby Lab, Department of Psychology, Uppsala University. A special infant chair was used for supporting the hips and lower trunk of the infant while leaving the upper part of the body and the arms free (Bumbo Ltd, Gauteng, South Africa). With a parent close behind, the infant was placed in front of a vertical screen, where a small toy (diagonal 4 cm) moved along a semicircular trajectory (radius 35 cm) with its lowest point in front and within reach (20 cm distance) of the infant. The starting point was randomly assigned either to the top right or top left of the trajectory, and the toy then moved with a sinusoidally modulated velocity with maximum velocity in front of the infant (24 cm/s). Two passive reflective markers were placed on each hand of the infant and one on the small toy. Five ProReflex cameras (Qualisys, Gothenburg, Sweden) were placed above and to the sides of the infant to capture the coordinates of the moving hands and toy at a recording frequency of 240 Hz (Fig. 1 Experimental set up). (Grönqvist et al., 2011). 2.3. Kinematic parameters Goal directed motor actions are planned in advance and corrected through visual control during the action. The planning of a reach is reflected in how close the aiming is relative to the goal (Fig. 2). The straightness, or relative length, of the movement is another aspect of planning. This measure refers to the ratio between the path (cm) that the hand actually travels towards the object, and the shortest possible path (cm) between start and goal. A reach is organized in terms of velocity pulses, called movement units (MU), each consisting of an acceleration and a deceleration phase (von Hofsten, 1991). Adults usually use one MU when implementing a reach, which means that the velocity of the hand increases at the beginning of the movement and decreases towards the end of it. Infants, however, typically build goal directed reaching movements in a series of MUs. The MU covering the largest part of the distance towards the object is most often positioned at the beginning of the reach with the subsequent MUs correcting for errors in the initial trajectory. Over the first year of life, infants use a decreasing number of MUs, indicating more mature planning and execution of the reach. As the transition between the MUs often coincides with change in direction of the reach, the number of MUs and the relative length of the reach are related. Other aspects of reaching quality is indicated by strategies used by the infant to obtain the goal, eagerness in trying to catch the object and successrates of grabbing it. 3
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Fig. 1. The infant is sitting in front of the screen with the moving object ready to reach out for it. Reflective markers are placed on both hands and on the object.
Fig. 2. Aiming measures how well the infant anticipate the future meeting point between the hand and the moving object. The object position as the reach starts is at position (a) and moves to position (b) as the reach ends. The angle formed by the position of the hand at the start (c) and the positions of the object at the start (a) and at the end (b) of the reach is called β, and the angle formed between the positions of the object (a) and hand (c) at the start and the hand at the end (d) of the reach is called α. For a perfect aim α-β should equal 0, and for a predictive reach the hand should arrive at the interception point ahead of the object, as indicated by a negative value.
A movement was defined as a reach when one or two hands started to move consistently towards the trajectory of the object for a distance of 7 cm or more. The infants reached for the object 14 times on average (range 2–28), the mean of which was used in the analysis. The experiment was terminated when the infant no longer showed an interest in the task. A bimanual coupled reach was defined when the two hands were coordinated in time, i.e. set out for the object less than .5 s from each other (Grönqvist, Brodd, von Hofsten, 2011). All kinematic varables constitute mean values for the individual child, exept where specified as number or 4
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proportion. Detailed descriptions of the kinematic reaching parameters at 8 months were published previously (Grönqvist, Brodd, von Hofsten, 2011). Thus, the variables aiming and relative length, which are related to planning, and MUs, which are an expression of visuomotor control, will be referred to as visuomotor planning. Reach execution will referre to strategies (unimanual or bimanual, proportion of bimanually coupled reaches, number of hits and attempts) and how successful the infant was at grasping the object. 2.4. Assessment of preschool neurodevelopment The children were tested with the BSID-III (Bayley, 2006) at around 2.5 years CA (mean 32 months, range 28–41) by a licensed psychologist at the Department of Paediatrics, Uppsala University Hospital. The psychologist was blinded to the reaching assessment results. Due to the need for calculating CA to administer the BSID-III correctly, it was not possible to be blinded to GA. The BSID-III provides estimates on five subscales: cognition, receptive and expressive language, and fine and gross motor function. 2.5. Statistical procedures Data were compiled in IBM SPSS Statistics for Windows, Version 22.0 (Armonk, NY: IBM Corp. USA), with regression analysis performed separetly in R (open sorce). For comparisons between the EPT and VPT groups, Student’s t-test or Fishers’ exact test were used for parametric and non- parametric data respectively. As the proportion of infants with specific neonatal complications was low, controlling for each of them separately was considered unfeasible. Tests of normal distribution were carried out with Shapiro-Wilk’s test. Because of heteroscedasticity, only some of the BSID-III sub scales met the criteria for parametric testing (Shapiro Wilkes, pvalues ranging between .002 and .66), and for the sake of uniformity, Spearman correlations were performed to test all associations between reaching parameters and BSID-III results. Non parametric analysis could not address the question about interaction effects, how BSID-III results were dependent on reaching parameters. After statistical advice we performed linear regression models, with the reservation that the data did not meet criteria for parametric testing and that the sample size was not sufficient for the number of predictors required. To compensate for the heteroscedasticity, robust confidence intervals and p-values were computed using the Bell-McCaffrey robust standard errors (Imbens & Kolesar, 2016) as implemented in the R package clubSandwich. The predictors included in the analysis were grouping by gestational age (EPT, VPT), aiming and its interaction with gestational age groupning, as well as proportion of bimanual coupled reaches and its interaction with gestational age grouping. The focus of the analysises were on the interaction terms, and five models were performed – one for each BSID-III subscale. The variables of aiming and proportion of bimanual coupled reaches were selected because of their complexity and cognitive demands. Also, proportion of bimanual coupled reaches was the parameter that had differed between the preterm infants in the cohort compared to full term controls (Grönqvist, Brodd, von Hofsten, 2011). 3. Results Data for visuomotor planning and reach execution, are shown in Table 1 as well as group values for the BSID-III results. As observed in Table 1, the infants in the EPT group had more neonatal clinical risk factors than the VPT born infants. However, comparisons of reaching parameters between the EPT and VPT groups, revealed no statistical differences (p-values ranging between .10 and .99). Moreover, the overall BSID-III subscores did not differ significantly between the EPT and VPT children (Table 1). The mean scores for cognition, receptive and expressive language, and fine motor function, respectively, were all within +/- 1 SD of the Swedish published reference values. The scores for gross motor function did not differ statistically between the two groups in this sample but for the EPT group they were clearly below Swedish reference data (Månsson & Stjernqvist, 2014). In comparison to the reference data, 16 children had at least one BSID result < -1 SD, and eight had two or more < -1 SD. Four children had at least one result < -2 SD. Table 2 Spearman’s correlations co-efficient (r) values for reaching parameters at 8 months corrected age and Bayley Scales of Infant and Toddler Development (BSID III) subscale scores as assessed at 2.5 years of corrected age in children born preterm. Only statistically significant results are depicted. ** p < .01, * p < .05, † p < .06. For definitions of kinematic parameters, please see section 2.3.
Visuomotor planning Aiming Relative length Movement units Reach execution Number of bimanual reaching attempts Proportion of bimanual reaching attempts Number of bimanual coupled reaches Proportion of bimanual coupled reaches Number of reaching attempts Number of failed reaching attempts
Cognition
Receptive language
−.39* .48**
−.44** .34*
Expressive language
Fine motor
Gross motor
.42* .33†
.37* .35* .33* .43** .36*
.39* .36*
.32† .31† .35*
.36* .36*
.36*
5
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Table 3 Spearman´s correlations co-efficient (r) values for reaching parameters at 8 months corrected age and Bayley Scales of Infant and Toddler Development (BSID-III) subscale scores as assessed at 2.5 years of corrected age in children born extremely preterm (gestational age < 28 weeks) and very preterm (gestational age 28–31 weeks). Only statistically significant results are depicted. **p < .01, *p < .05, † p < .06. EPT, n = 13
Visuomotor Planning Aiming Relative length Movement units Reach execution Number of hits Number of reaching attmepts Number of bimanual hits Proportion of bimanual coupled reaches Number of bimanual coupled reaches
VPT, n = 23
Cognition
Receptive Language
Expressive Language
−.77** .74** .68*
−.65* .64* .55*
−.62* .71** .58*
Fine Motor
Gross Motor
Cognition
Receptive Language
Expressive Language
Fine motor
Gross Motor
−.50*
.52* .40†
.54**
.42*
.51* .65**
.43*
.61**
.43*
.41†
For the whole group of children, several reaching parameters at 8 months were related to neurodevelopment at 2.5 years, especially for cognition and the receptive language subscale (Table 2). A better visuomotor planning and reach execution related to higher cognitive and language subscale scores. The parameters that showed the highest correlations were relative length, aiming, and the proportion of bimanual coupled reaches. Fewer associations were found for reaching parameters and fine- and gross motor scores (Table 2). For the reach execution parameters (number of attempts, bimanual reaches, and coupled reaches as well as proportion of bimanual coupled reaches), all significant associations were positive indicating that the more attempts to obtain the object, the more bimanual strategies were used and the higher the success rate – the better the neurodevelopmental outcome. In addition, the regression models indicate interaction effects for aiming and gestational age grouping, for cognition (p = .056) and for expressive language (p = .095) although not reaching statistical significance. When split into sub groups according to gestational age, the patterns of associations between reaching parameter and BSID subscales differed between EPT and VPT infants (Table 3). Importantly, reaching data variance was similar in the two groups. In the EPT group, aiming, relative length, and number of MUs correlated significantly with BSID scores for cognition and language. In the VPT group, the total number of attempts, coupled reaches, hits and bimanual hits were associated with cognition, and receptive and expressive language.In the VPT group, there were also correlations between aiming and BSID fine motor function scores, and between number of hits and BSID gross motor scores. Within the EPT group, the number of MUs correlated with aiming (r = .56, p = .03) and relative length (r = .86, p < .001). In the VPT group, relative length and number of MUs and relative length were interrelated (r = .63, p < .001) but neither of these parameters were related to aiming. 4. Discussion Aspects of visuomotor planning and control, as well as of reach execution were both connected to outcome. Kinnematics relevant to planning the reach in advance, such as aiming and relative length were related to cognitive, language and fine motor outcome. The use of both hands in coordination was related to several of the later outcome measures. This was more important than how often the infant succeeded in catching the object. Successful reaching gives the infant an opportunity for exploration, which has been shown to give a cascading effect on later academic achievement in typically developing children (Bornstein, Hahn, & Suwalsky, 2013). The relationship has been confirmed in children born extremely preterm (< 28 GW) children up to two years of age (Zuccarini et al., 2017). Importantly, the relationship between early reaching and later neurodevelopment differed between EPT and VPT infants. In EPT infants, the visuomotor planning and control of reaching correlated strongly with later cognition and language scores at 2.5 years. In contrast, the relationship between reaching and neurodevelopment in the VPT children was reflected in the executional aspects of reaching. In addition, indications of interaction effects between aiming and gestational age grouping on cognition and expressive language suggest that cognitive and expressive language scores was not affected by aiming for the VPT group but for the EPT group higher cognitive and expressive laguage score was indicated by a more predictive aim. Somewhat surprisingly, the results suggest that the EPT infants with more MUs and a more circuitous reaching trajectory, also aimed their reaches further ahead of the moving object and had higher scores on the neurodevelopmental assessment. Being ahead of the object is a better strategy for a successful reach than lagging behind because it allows slowing down of the hand to meet the object. In contrast, a lagging reach necessitates speeding up and chasing the object. In other words, being ahead is advantageous 6
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because it gives extra time for zooming in on the object, giving rise to more MUs. However, this strategy may also be associated with later motor problems, which could explain the abscence of associations to later motor results on the BSID-III. Subjects who are motorically disadvantaged are expected to have a more circuitous reaching trajectory and have more MUs to compensate for this. Forsström and von Hofsten (1982) found that children with neurological impairments consistently aimed their reaches more ahead of the object as compared to typically developing children, and the relative lengths of their reaches were larger. In the LOVIS cohort, the infants who had a more pronounced neuromotor deficit at 10 months, aimed further ahead than infants with better neuromotor function (Grönqvist, Brodd, von Hofsten, 2011). A previous comparison of the very preterm infants with full term infants in Grönqvist, Brodd, von Hofsten (2011) showed that both groups were on average equally successful in catching a moving object, but the preterm infants used more bimanual reaches. The present results suggest advantages for the preterm infants with more bimanual reaching. The suggested relationships between individual reaching parameters and neurodevelopment may in part be due to differences in motor development that prevail during the first year of life in infants born EPT as compared to those who are VPT and/or without neonatal complications (Montgomery, Hellström-Westas, Strand Brodd, Sonnander, & Persson, 2017). Schneider et al. (2008) found an impairment in programming of visuomotor uni- and bi-manual tasks at 8 years for children born EPT, but not for children born at later gestational ages. The present results show that early visuomotor skills in infants born very preterm are closely related to later cognitive abilities. These findings are in agreement with Kaul, Rosander, von Hofsten, Brodd, Holmström, Kaul, et al., 2016 who demonstrated that gaze tracking at 4 months CA is related to neurodevelopment at 2.5 years of age. As hypothesized, reaching for moving objects showed a stronger relationship to later cognitive development than studies of reaching for stationary objects (Fallang et al., 2003, Fallang et al., 2005). Another study comparing reaching for moving objects in preterm and full term infants (van der Meer, van der Weel, Lee, Laing, & Lin, 1995) found a delay in onset of reaching and in choice of most effective strategy for the preterm group. The infants who had not switched to the more effective strategy at 48 weeks were later diagnosed with CP. The authors conclude, that a catching task could be useful in detecting brain damage. To catch a moving object, we rely on internal models of events that have not yet occurred. This process has similarities with expressive language (Ellis, Robledo Gonzalez, & Deák, 2014). In addition, a connection between early motor function and later communicative skills has been demonstrated in extremely preterm infants (Benassi et al., 2016). Also, parental ratings and observational studies of gestures, pointing and object manipulation in children born preterm further support to the idea that through early motor development the infant gets new opportunities to refine skills that are shared between numeous functions, including language (Iverson, 2010). It is argued that several constraints are posed by prematurity on the development of the infant, where alterations in motor, perceptual and communicative functions limits the typical development of language (Sansavini et al., 2011; Stolt et al., 2014; Zuccarini et al., 2018). A recent study by Gottwald, Achermann, Marciszko, Lindskog, and Gredebäck (2016) established the relation between kinematics of reaching and executive functioning in a group of healthy 18 month-old toddlers. The velocity peak of the first MU was related to inhibition and working memory on concurrent tasks. Our results connect reaching parameters at 8 months to neurodevelopment at later ages, further supporting the idea that reaching could be an early executive function marker and that motor control and executive function early in life could share a common base. In line with a number of experimental studies on visuomotor processing in premature infants (Atkinson & Braddick, 2011) the present data are interpreted according to dorsal stream vulnerability. They (Atkinson & Braddick, 2007; Braddick, Atkinson, & Wattam-Bell, 2011) found evidence that impairments of the dorsal visual pathways in infants born preterm are associated with an increased risk of motor disturbance and cognitive deficits. Taken together, our data (Table 3) indicate that the development of visual control of reaching in EPT and VPT follow different patterns. The indication is that in EPT children, basic motion perception and prediction of action goals are affected and in VPT children the coordination of bimanual actions. Bimanual reaching reflects a different aspect of the dorsal process than the planning itself. It is about coordinated sequences in time that goes beyond simple transformation of visuospatial information, and has been found to be sensitive to white matter damage (Birtles, Anker, Atkinson, Shellens, Briscoe, Mahoney, et al., 2011). Most mean BSID-III results for both the EPT and the VPT children are within +- 1 SD of the age equivalent EXPRESS study control group (Månsson & Stjernqvist, 2014) and when EPT and VPT groups of the present study are compared, no average differences between the kinematic data or BSID results are found. It is remarkable that the BSID-III results are so good on the average in both groups. The selection of the participants excluding severe braindamage or the inherent properties of the BSID-III, may in part explain this finding. It should also be noted, that neonatal riskfactors are more common within the EPT group. For understanding the developmental impact of extreme prematurity the infants abilities should be measured at two or more occasions as meassurments are similar between groups at both assessment points, but in relations between the two differences appear. The present study indicate that if the EPT infants are less matured than the VPT at 8 months the difference persists at 2.5 years. 5. Conclusion The different associations between reaching parameters and neurodevelopment indicate that several maturational processes may be involved in early reaching influence neurodevelopment. For the control of reaching for moving objects in the EPT children, more basic problems prevail that depend on how motion information is incorporated with action planning. For the VPT children, coordination of bimanual coupled reaches is more at the focus. The findings may be used for differentiating interventions with respect to GA. 7
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Funding Financial support was obtained from the Queen Silvia´s Jubilee Foundation, Stockholm, Sweden; the Linnéa and Josef Carlsson Foundation, Helsingborg, Sweden; the Jerring Foundation, Stockholm, Sweden; the Gillbergska Foundation, Uppsala, Sweden and the Swedish Research Council (2009-1093) and (2016-03109). None of the funders have in any way been involved in any step of the study. Acknowledgements We thank all children and parents who participated in the study. We also acknowledge the work by the following: professor Uwe Ewald, associate professor Bo Strömberg, professor Gerd Holmström, associate professor Pär Nyström, associate professor Olga Kochukhova, psychologist Ingela Helling. Special thanks to Lars Lindhagen for statistical consultations. References Atkinson, J., & Braddick, O. (2007). Visual and visuocognitive development in children born very prematurely. Progress in Brain Research, 164, 123–149. https://doi. org/10.1016/S0079-6123(07)64007-2. 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