Toddlers actively reorganize their whole body coordination to maintain walking stability while carrying an object

Gait & Posture 50 (2016) 75–81

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Toddlers actively reorganize their whole body coordination to maintain walking stability while carrying an object Wen-Hao Hsua,* , Daniel L. Mirandaa , Trevor L. Chistolinia,b , Eugene C. Goldfielda a b

Wyss Institute for Biologically Inspired Engineering at Harvard University, 3 Blackfan Circle, 2nd Floor, Boston, MA 02115, USA Harvard University, Massachusetts Hall, Cambridge, MA 02138, USA

A R T I C L E I N F O

Article history: Received 28 April 2016 Received in revised form 26 July 2016 Accepted 23 August 2016 Keywords: Gait Coordination Object carriage Child development

A B S T R A C T

Balanced walking involves freely swinging the limbs like pendula. However, children immediately begin to carry objects as soon as they can walk. One possibility for this early skill development is that whole body coordination during walking may be re-organized into loosely coupled collections of body parts, allowing children to use their arms to perform one function, while the legs perform another. Therefore, this study examines: 1) how carrying an object affects the coordination of the arms and legs during walking, and 2) if carrying an object influences stride length and width. Ten healthy toddlers with 3–12 months of walking experience were recruited to walk barefoot while carrying or not carrying a small toy. Stride length, width, speed, and continuous relative phase (CRP) of the hips and of the shoulders were compared between carrying conditions. While both arms and legs demonstrated destabilization and stabilization throughout the gait cycle, the arms showed a reduction in intra-subject coordination variability in response to carrying an object. Carrying an object may modify the function of the arms from swinging for balance to maintaining hold of an object. The observed period-dependent changes of the inter-limb coordination of the hips and of the shoulders also support this interpretation. Overall, these findings support the view that whole-body coordination patterns may become partitioned in particular ways as a function of task requirements. ã 2016 Elsevier B.V. All rights reserved.

1. Introduction Young children learn the many possible combinations of body articulators that may be used to explore their environments as well as perform more goal-directed tasks [1,2]. One of the major challenges in early childhood is discovering how to perform one action with the legs (e.g., locomotion) while simultaneously performing another action with the hands (e.g., manipulating objects). Children learn very early in life to preferentially use the upper body for more differentiated and skilled actions. Particularly, a walking child has free use of their hands for exploring the environment. This ability may play a role in partitioning a global pattern of swinging arms and legs into a variety of more loosely coupled ways of using their hands while locomoting. The differentiated function of the hands is already apparent during infancy. For example, we conducted a longitudinal study of the differentiation of arms and legs in infants between the ages of 3 and 6 months, when they were presented with an overhead mobile

* Corresponding author. E-mail address: [email protected] (W.-H. Hsu). http://dx.doi.org/10.1016/j.gaitpost.2016.08.023 0966-6362/ã 2016 Elsevier B.V. All rights reserved.

[3]. For arm movements, the joint rotation of shoulders and elbows became more weakly coordinated from 3 to 6 months. By contrast, no consistent coordination changes were found between the hips and knees. Furthermore, the arms and legs were moving in more functionally independent patterns by 6 months of age. These infants were more likely to keep their hands away from the body to reach midline objects while moving their feet close to the body to maximize kicks. These findings suggest that the relaxation of coordination between joints may be a precursor for the functional differentiation between arms and legs during infancy and early childhood. Another opportunity to examine the process of functional differentiation of arms and legs is the transition from crawling to walking. At this transition, children no longer need to use their upper extremities as support but are able to swing their arms freely in space during walking. Arm swing is important for walking stability because it reduces vertical angular moment, vertical ground reaction moment, and energy consumption [4]. Furthermore, walking increases children’s ability to physically interact with the environment [5], allowing them, for example, to carry objects [6]. In order to walk and carry objects at the same time, children need to assemble a set of functional units for locomotion

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and another set for carrying. Although children younger than 2 years old tend to employ a less mature, high guard posture while carrying objects during walking, their balance appears to be unaffected [7]. In fact, children fall less when carrying objects than when not carrying objects [6]. Children seem to be able to use their arms and legs to stabilize themselves during walking while simultaneously carrying objects. One possibility is that a relaxation in the coordination of the larger functional units of the upper and lower body allows children to perform these separate functions at the same time. Surprisingly, there have been few studies investigating how the coordination of the arms is modified in response to carrying objects during walking, where the dominant coordination patterns involve the functional units of the legs. Therefore, questions remain about how carrying objects affects inter-limb coordination of the arms and legs. To begin to address these questions, we measure the coordination pattern and stability between two segments by calculating their continuous relative phase (CRP) [8]. Furthermore, as opposed to quantifying the overall coordination of the gait cycle, it is possible to separate the gait cycle into phases to further analyze important transition periods. For example, the transitions from double limb support to single limb support during stance and from accelerating to decelerating the leg during swing may require different coordination to maintain stability during gait. Our goal in this study was to determine the coordination by which children use their arms and legs for walking while simultaneously performing carrying. To answer this question, we set out to determine: 1) how carrying an object affects the coordination of the arms and legs during walking, and 2) if carrying an object influences stride length, width, and speed. We hypothesized that carrying a small object would change coordination patterns as measured by CRP during different periods of the gait cycle when the arms may play a greater role in locomotion, allowing them to both stabilize gait and perform the carrying function. Furthermore, we hypothesized that carrying a small object would not affect stride length, width, or speed. 2. Methods 2.1. Participants Ten healthy, typically developing children with 3–12 months of walking experience, reported by parent or legal guardian, participated in this study (Table 1). The criterion of 3–12 months walking experience was chosen to reduce the occurrence of high guard posture during walking, as evidence suggests that children have lowered their arms after 10 weeks of walking [9]. Furthermore, between 3 and 12 months of walking experience, the development of walking ability transitions from being related to developing a skillset to fine tuning those skills with experience Table 1 Participant characteristics. Participant ID

Sex

01 02 03 04 05 06 07 08 09 10 Mean (SD)

M M F M M M M F M M

Age (month)

Height (m)

Weight (kg)

Walking Experience (month)

20 14 27 18 20 29 27 20 14 24 21.3 (5.3)

0.80 0.72 0.86 0.78 0.84 0.92 0.86 0.80 0.78 0.83 0.82 (0.06)

13.4 11.2 12.8 11.2 10.7 15.0 11.9 10.0 10.1 11.2 11.8 (1.6)

9 4 9 5 10 11 9 4 3 12 7.6 (3.3)

[10,11]. Each child participated in one visit after the parent provided written informed consent. All experimental procedures and recruitment materials used for this study were approved by Harvard Medical School and Boston Children's Hospital Institutional Review Boards. 2.2. Procedure Two 30  30  30 cm bins were placed 4 m apart in the center of the motion capture lab. Each bin contained various small and lightweight (30 g) toys. We chose small toys because young children tend to carry objects smaller than their hands during walking [6]. Retroreflective surface markers were placed on each participant’s body (Fig. 1). A nine-camera T-Series Vicon (Centennial, CO) motion capture system was positioned around the lab to track the markers at a sampling rate of 120 Hz. Each participant was asked to stand barefoot next to one of the bins to either: 1) pick up a toy from the closest bin then walk toward and put the toy in the other bin (one-object carrying condition); or 2) walk toward the other bin to pick up a toy (no-object carrying condition). The parent and one of the researchers were sitting next to each bin to encourage the participant to walk. Ten to fifteen successful walking trials, where the participant walked from one bin to the other without falling, were recorded for further analysis. 2.3. Data process and analysis The retroreflective marker data were labeled using Vicon Nexus 1.8.5 software (Centennial, CO) and then processed using Visual3D v5 software (C-Motion, Germantown, MD). Kinematic data were filtered using a 4th-order lowpass Butterworth filter with a cutoff frequency of 6 Hz. A 15-segment kinematic model was built for each participant (Fig. 1). Sagittal plane joint angles were calculated for the hips and shoulders using methods present by Grood and Suntay [12], and Wu et al. [13,14]. The gait events of heel strike (HS) and toe-off (TO) for the left and right strides were determined using algorithms proposed by Hreljac and Marshall [15]. In the one-object carrying condition, only trials when the participants held a toy in one hand were included for analysis. Any trials with visible changes in the walking direction were excluded. Twenty

Right Head Anterior Head

Le Head

Right Shoulder

Le Shoulder

Right Medial Elbow

Le Lateral Elbow

Right Lateral Elbow

Le Medial Elbow

Right Medial Wrist

Le Lateral Wrist

Right Lateral Wrist

Le Hand

Right Hand

Le Medial Wrist

Right Iliac Crest

Le Iliac Crest

Right Hip

Le Hip

Right Medial Knee

Le Medial Knee

Right Lateral Knee

Le Lateral Knee

Right Medial Ankle

Le Medial Ankle

Right Lateral Ankle

Le Lateral Ankle

Right Foot

Le Foot

Fig. 1. Illustration of the placement of the retroreflective markers on the 15segment model. Markers were placed on the body landmarks of the head, torso, pelvis, and upper and lower extremities. The 15-segment model includes the head, torso, pelvis, and the left and right upper arms, lower arms, hands, thighs, shanks and feet.

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strides, 10 from each side, of kinematic data were extracted for each carrying condition. The average walking speed in each carry condition was measured from these strides. Each participant’s mean stride length and width, normalized by leg length (L), were calculated for each carrying condition. Inter-limb coordination of the hips and shoulders during walking was measured by calculating CRP [8]. First, the stride-bystride hip and shoulder joint angles were time normalized to the gait cycle with 101 points. CRP angles between left and right hips, and left and right shoulders were then measured for all participants’ kinematic data using custom MATLAB R2016a software (The MathWorks, Natick, MA). CRP angles range from 180 to 180 , where 0 represents an in-phase coordination and

(A)

No−Object

180 represents an out-of-phase coordination. For each participant, the mean CRP angles and the intra-subject variability (standard deviation) of the mean CRP angles at each percentage of the gait cycle for the right strides were calculated using circular statistics [16]. The mean absolute relative phase (MARP) and deviation phase (DP) of the hips and shoulders over the periods of interest were calculated to characterize and compare the phase relationship and variability of the CRP angle curves using simple descriptive statistics, respectively [17]. Herein, the right gait cycle was separated into the stance and swing phases, using HS and TO events as the cutoff. The stance phase was then divided into initial double limb support (ST1, from right HS to left TO), single limb support (ST2, from left TO to left HS) and terminal double limb

(D)

Right Hip Joint Angle 80 One−Object

Angle (°) Ext <−−> Flex

Angle (°) Ext <−−> Flex

20 0 −20

Right Shoulder Joint Angle 80 No−Object

60

60 40

20 0 −20 −40

ST1 0

ST2 20

40

ST3

SW1

60

80

SW2

−60

100

ST1 0

ST2 20

Left Hip Joint Angle No−Object

(E)

One−Object

Angle (°) Ext <−−> Flex

Angle (°) Ext <−−> Flex

40 20 0

SW1

60

SW2

80

100

Left Shoulder Joint Angle No−Object

One−Object

40 20 0 −20 −40

ST1 0

ST2 20

40

ST3

SW1

60

80

SW2

−60

100

ST1 0

ST2 20

Gait Cycle (%)

(C)

(F)

CRP Angle Between Hips* No−Object

40

ST3

SW1

60

SW2

80

100

Gait Cycle (%)

−100

CRP Angle Between Shoulders* 300

One−Object

No−Object

One−Object

250

−150

Phase Angle (°)

Phase Angle (°)

ST3

80 60

60

−200

−250

−300

40

Gait Cycle (%)

80

−20

One−Object

40

Gait Cycle (%)

(B)

77

200 150 100

ST1 0

ST2 20

40

ST3

SW1

60

Gait Cycle (%)

80

SW2 100

50

ST1 0

ST2 20

40

ST3

SW1

60

80

SW2 100

Gait Cycle (%)

Fig. 2. The mean (A) right hip joint angle, (B) left hip joint angle, (C) continuous relative phase (CRP) angle of the hips, (D) right shoulder joint angle, (E) left shoulder joint angle, and (F) CRP angle of the shoulders during the right gait cycle in both no-object and one-object carrying conditions for all participants. Black solid lines represent angles in no-object carry condition and gray dashed lines represent angles in one-object carry condition. Standard deviation of each curve is shown as the shaded area. Angles are normalized to the right gait cycle where 0% occurs at the right foot heel strike and 100% occurs at the next right foot heel strike. Vertical solid lines represent the right foot toeoff event, dividing the gait cycle into the stance and swing phases. Vertical dotted lines separate the stance phase and swing phase into initial double limb support (ST1), single limb support (ST2), and terminal double limb support (ST3) periods, and swing acceleration (SW1) and swing deceleration (SW2) periods, respectively. *For visual purpose, curves are smoothed by shifting any discontinuous regions with 360 .

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support (ST3, from left HS to right TO) periods [18]. The swing phase was divided equally into early and late periods, which represent the swing acceleration (SW1) and deceleration (SW2), respectively. The MARP was calculated by averaging the absolute values of the ensemble curve for each period. A MARP value close to zero indicates a more in-phase coordination between the two segments. The DP was calculated by averaging the standard deviations of the ensemble curve for each period. A low DP value indicates a more stable coordination between the two segments. 2.4. Statistical analysis Statistical analyses were performed using GraphPad Prism 6 (GraphPad Software, La Jolla, CA). Children demonstrate high variability in their kinematics during activities [19,20], and it is important to control individual differences when we determine how carrying an object affects the coordination of the arms and legs during walking. Therefore, a repeated measures analysis of variance (ANOVA) with 1) carrying condition (no-object and oneobject), and 2) period (ST1, ST2, and ST3 for the stance phase; SW1 and SW2 for the swing phase) factors, was applied to the MARP and DP within each phase of the hips and of the shoulders separately. A paired samples t-test with carrying condition (no-object and oneobject) factor was applied to stride length, width, and speed results. These analyses allowed us to use each individual as his/her

(A)

NO-OBJECT

3. Results The mean joint angle, CRP angle, and variability of the CRP angle of the hips and shoulders in both carrying conditions for all participants are shown in Fig. 2. The MARP and DP results between conditions for the hips and shoulders during the stance and swing phases are presented in Figs. 3 and 4, respectively. No differences were observed between conditions in stride length (no-object: 1.32  0.20 m/L; one-object: 1.38  0.22 m/L), width (no-object: 0.26  0.06 m/L; one-object: 0.25  0.06 m/L), or speed (no-object: 0.72  0.22 m/s; one-object: 0.82  0.16 m/s). There were significant differences between periods in the DP of the 1) shoulders during the stance phase (ST1: 58.5  10.3 ; ST2: 48.0  13.4 ; ST3: 42.6  17.8 ; ES = 0.61; p < 0.01) (Fig. 3D); and 2) hips during the swing phase (SW1: 18.4  7.3 ; SW2: 13.9  3.9 ; ES = 0.44; p = 0.03) (Fig. 4C). In addition, there were interactions between conditions and periods in the 1) MARP of the hips during the stance phase (ES = 0.47; p < 0.01) (Fig. 3A); and 2) DP of the shoulders during the swing phase (ES = 0.63; p < 0.01)

(C)

Hips MARP 200

own control [21]. Statistical significance was set at an alpha level of 0.05. Additionally, the effect size (ES) was calculated to measure the magnitude of difference for all variables. An effect size of 0.2 is considered a small effect, 0.5 is considered a medium effect, and 0.8 is considered a large effect [21].

ONE-OBJECT

*** p = 0.04

40

** p < 0.01 *** p = 0.04

NO-OBJECT

100

50

20

10

INITIAL DOUBLE LIMB SUPPORT (ST1)

SINGLE LIMB SUPPORT (ST2)

0

TERMINAL DOUBLE LIMB SUPPORT (ST3)

INITIAL DOUBLE LIMB SUPPORT (ST1)

Period

(B)

ONE-OBJECT

30

DP (°)

MARP (°)

150

0

Hips DP

NO-OBJECT

TERMINAL DOUBLE LIMB SUPPORT (ST3)

Period

Shoulders MARP 250

SINGLE LIMB SUPPORT (ST2)

ONE-OBJECT

Shoulders DP

(D) 80

NO-OBJECT

ONE-OBJECT * p < 0.01

200

150

DP (°)

MARP (°)

60

40

100 20

50

0

0 INITIAL DOUBLE LIMB SUPPORT (ST1)

SINGLE LIMB SUPPORT (ST2)

Period

TERMINAL DOUBLE LIMB SUPPORT (ST3)

INITIAL DOUBLE LIMB SUPPORT (ST1)

SINGLE LIMB SUPPORT (ST2)

TERMINAL DOUBLE LIMB SUPPORT (ST3)

Period

Fig. 3. Bar graphs containing the results for the (A) hips MARP, (B) shoulders MARP, (C) hips DP, and (D) shoulders DP in the stance phase. Black bars represent variables in noobject carrying condition and gray bars represent variables in one-object carrying condition. Error bars represent one standard deviation of the measured variables. * denotes significant differences between periods. ** denotes interactions between periods and carrying conditions. *** denotes significant differences between carrying conditions.

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(A)

(C)

Hips MARP

200

NO-OBJECT

ONE-OBJECT

79

Hips DP NO-OBJECT

40

ONE-OBJECT * p = 0.03

30

DP (°)

MARP (°)

150

100

20

10

50

0

0 SWING ACCELERATION (SW1)

SWING ACCELERATION (SW1)

SWING DECELERATION (SW2)

Period

Period

Shoulders MARP

(B) 250

NO-OBJECT

SWING DECELERATION (SW2)

Shoulders DP

(D)

ONE-OBJECT

NO-OBJECT

80

ONE-OBJECT

** p < 0.01

*** p = 0.03 200

150

DP (°)

MARP (°)

60

40

100 20 50

0

0 SWING ACCELERATION (SW1)

SWING DECELERATION (SW2)

SWING ACCELERATION (SW1)

Period

SWING DECELERATION (SW2)

Period

Fig. 4. Bar graphs containing the results for the (A) hips MARP, (B) shoulders MARP, (C) hips DP, and (D) shoulders DP in the swing phase. Black bars represent variables in noobject carrying condition and gray bars represent variables in one-object carrying condition. Error bars represent one standard deviation of the measured variables. * denotes significant differences between periods. ** denotes interactions between periods and carrying conditions. *** denotes significant differences between carrying conditions.

(Fig. 4D). Post hoc multiple comparisons showed that, for the hips, the MARP for the one-object condition was lower than the noobject condition during the ST1 period (no-object: 160.2  13.3 ; one-object: 152.3  14.2 ; p = 0.04). Furthermore, the MARP of the hips for the one-object condition was higher than the no-object condition during the ST3 period (no-object: 139.8  22.5 ; oneobject: 147.7  25.6 ; p = 0.04). Lastly, during the SW1 period, the shoulders were more variable for the no-object carrying condition than the one-object carrying condition (no-object: 52.3  16.6 ; one-object: 46.8  11.8 ; p = 0.03). In summary, carrying an object did not influence stride length, width, or speed. However, carrying an object 1) affected hips interlimb coordination during the double limb support periods of the stance phase; and 2) reduced the intra-subject variability of the shoulders during the swing acceleration period when compared to the no-object carrying condition. Furthermore, the hips during the early period of the swing phase and the shoulders during the early period of the stance phase demonstrated a higher variability when compared to the remaining periods of the swing and stance phases, respectively.

4. Discussion We have examined how toddlers coordinate the upper body to perform carrying while the lower body performs walking. Our hypotheses were that carrying a small object would influence arm and leg coordination patterns during different periods of the gait cycle but would not affect stride length, width, or speed. Overall, both the hips and the shoulders demonstrated out-of-phase interlimb coordination (CRP  180 ) throughout the stance and swing phases (Fig. 2C and F) regardless of carrying condition, which represents the typical rhythmic coordination of the limbs in bipedal walking (see Meyns et al. [22] for typically developing children data). The analysis on intra-subject inter-limb coordination of the hips and shoulders showed that the coordination of the 1) hips during the swing acceleration period, and 2) shoulders during the initial double limb support period of the stance phase were more variable than the remaining periods of the swing and stance phases, respectively. These period-dependent changes indicate destabilization and stabilization of the inter-limb coordination of the hips and of the shoulders throughout the gait cycle. Specifically, the inter-limb coordination of the hips and of the shoulders becomes more variable around the periods when the body weight is transferred from one foot to the other and the center of mass velocity is being redirected [23]. Later, the

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coordination becomes more stable during the remaining periods of the gait cycle. The analysis on inter-limb coordination of the hips and shoulders also showed that carrying an object did not affect the coordination of the shoulders during the stance phase. However, carrying an object reduced the intra-subject coordination variability of the shoulders during the swing acceleration period, indicating further stability was provided to arm swing. Because arm swing has been shown to benefit walking balance [4], a stable coordination of the shoulders during this period could be important for balance when step-to-step transitions occur. By contrast, in the hips, carrying an object affected the inter-limb coordination during the initial and terminal double limb support periods of stance. Nevertheless, such small changes in MARP (on average, about 8 ) in either period may not represent any drastic coordination change (i.e. switching from out-of-phase to in-phase) as the hips demonstrated out-of-phase inter-limb coordination through stance. Furthermore, DP in the three periods of stance was not affected by carrying condition. This indicates that inter-limb coordination of the legs has become entrenched and is able to remain stable during walking despite variation in arm function. Similar research shows that young children can coordinate their limbs in a not perfectly coupled but relatively stable fashion while performing dual motor task [24]. As children get older, the limbs couple even more and the variability in coordination decreases. Lastly, similar to the findings of Mangalindan et al. [7], our results showed that carrying an object did not affect stride length or width. These findings suggest that carrying small and light objects does not influence gait characteristics; albeit, children’s gait could be affected with heavier loads (15% of body weight) placed on the trunk symmetrically [25]. Nevertheless, children prefer to carry small and light objects during daily activities in early walking [6]. In summary, while both arms and legs demonstrated destabilization and stabilization throughout the gait cycle, the arms showed a reduction in intra-subject coordination variability in response to carrying an object. This reduction in variability may ultimately bolster the dynamic balance of a child while they walk. Since the arms and legs acted as coordinated segments for the function of walking, the system may modify the coordination as a means for maintaining the organization of this function while performing another one, such as carrying. These findings further support the evidence of the development of functional differentiation between arms and legs during infancy [3]. With the evolution of our opposable thumbs, there may have been selective pressures for this specialization of the hands, with more limited use of the feet for grasping. This evolutionary trend may function during ontogeny to impose certain constraints on learning to use the arms and legs for different tasks, such as throwing objects [26], carrying food [27,28], tools [29], or children [30] during walking. There are some limitations to this study. First, each child participated in only one visit. Children tend to demonstrate high kinematic variability (both intra- and inter-subject) during activities; however, by controlling for individual differences in our analysis we showed promising findings [19,20]. A longitudinal study with multiple visits may provide insight into the development of inter-limb coordination when children carry objects at different ages and the evolution of the inter-subject variability when children are at different ages. Furthermore, children were limited to carrying a small object in this study. While children prefer carrying small objects during early walking [6], future work should address how carrying objects of various sizes and weights affect coordination of the limbs during walking.

5. Conclusion Our findings reveal period-dependent destabilization and stabilization of the inter-limb coordination throughout the gait cycle as body weight shifts from one foot to the other, suggesting differential effects of step-to-step transition during walking. This supports the hypothesis that when young children carry an object, the whole body coordination may be actively reorganized to keep the upper body stable for carrying an object while still maintaining the gait cycle. The findings also suggest a more general hypothesis that whole body coordination may be partitioned in different ways for simultaneously performing multiple functions. Acknowledgement This study was funded by the Wyss Institute for Biologically Inspired Engineering at Harvard University. References [1] E. Thelen, J.A.S. Kelso, A. Fogel, Self-organizing systems and infant motor development, Dev. Rev. 7 (1987) 39–65, doi:http://dx.doi.org/10.1016/02732297(87)90004-9. [2] E. Thelen, B.D. Ulrich, P.H. Wolff, Hidden skills: a dynamic systems analysis of treadmill stepping during the first year, Monogr. Soc. Res. Child Dev. 56 (1991) i, doi:http://dx.doi.org/10.2307/1166099. [3] W.H. Hsu, D. Miranda, D. Young, K. Cakert, M. Qureshi, E. Goldfield, Developmental changes in coordination of infant arm and leg movements and the emergence of function, J. Mot. Learn. Dev. 2 (2014) 69–79, doi:http:// dx.doi.org/10.1123/jmld.2013-0033. [4] S.H. Collins, P.G. Adamczyk, A.D. Kuo, Dynamic arm swinging in human walking, Proc. R. Soc. B Biol. Sci. 276 (2009) 3679–3688, doi:http://dx.doi.org/ 10.1098/rspb.2009.0664. [5] K.E. Adolph, C.S. Tamis-LeMonda, The costs and benefits of development: the transition from crawling to walking, Child Dev. Perspect. 8 (2014) 187–192, doi:http://dx.doi.org/10.1111/cdep.12085. [6] L.B. Karasik, K.E. Adolph, C.S. Tamis-LeMonda, A.L. Zuckerman, Carry on: spontaneous object carrying in 13-month-old crawling and walking infants, Dev. Psychol. 48 (2012) 389–397, doi:http://dx.doi.org/10.1037/a0026040. [7] D.M.J. Mangalindan, M.A. Schmuckler, S.-A. Li, The impact of object carriage on independent locomotion, Infant Behav. Dev. 37 (2014) 76–85, doi:http://dx. doi.org/10.1016/j.infbeh.2013.12.008. [8] M.J. Kurz, N. Stergiou, Effect of normalization and phase angle calculations on continuous relative phase, J. Biomech. 35 (2002) 369–374, doi:http://dx.doi. org/10.1016/S0021-9290(01)00211-1. [9] C.N. Burnett, E.W. Johnson, Development of gait in childhood: part II, Dev. Med. Child Neurol. 13 (1971) 207–215, doi:http://dx.doi.org/10.1111/j.14698749.1971.tb03246.x. [10] S. Kingsnorth, M.A. Schmuckler, Walking skill versus walking experience as a predictor of barrier crossing in toddlers, Infant Behav. Dev. 23 (2000) 331–350, doi:http://dx.doi.org/10.1016/S0163-6383(01)00048-0. [11] B. Bril, Y. Brenière, Postural requirements and progression velocity in young walkers, J. Mot. Behav. 24 (1992) 105–116, doi:http://dx.doi.org/10.1080/ 00222895.1992.9941606. [12] E.S. Grood, W.J. Suntay, A joint coordinate system for the clinical description of three-dimensional motions: application to the knee, J. Biomech. Eng. 105 (1983) 136–144, doi:http://dx.doi.org/10.1115/1.3138397. [13] G. Wu, S. Siegler, P. Allard, C. Kirtley, A. Leardini, D. Rosenbaum, et al., ISB recommendation on definitions of joint coordinate system of various joints for the reporting of human joint motion—part I: ankle, hip, and spine, J. Biomech. 35 (2002) 543–548, doi:http://dx.doi.org/10.1016/S0021-9290(01)00222-6. [14] G. Wu, F.C.T. van der Helm, H.E.J. Veeger, M. Makhsous, P. Van Roy, C. Anglin, et al., ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion—Part II: shoulder, elbow, wrist and hand, J. Biomech. 38 (2005) 981–992, doi:http://dx.doi.org/ 10.1016/j.jbiomech.2004.05.042. [15] A. Hreljac, R.N. Marshall, Algorithms to determine event timing during normal walking using kinematic data, J. Biomech. 33 (2000) 783–786, doi:http://dx. doi.org/10.1016/S0021-9290(00)00014-2. [16] E. Batschelet, Circular Statistics in Biology, Academic Press, London, 1981. [17] N. Stergiou, S.D. Scholten, J.L. Jensen, D. Blanke, Intralimb coordination following obstacle clearance during running: the effect of obstacle height, Gait Posture 13 (2001) 210–220, doi:http://dx.doi.org/10.1016/S0966-6362(00) 00101-6. [18] J. Perry, Gait Analysis: Normal and Pathological Function, SLACK, Thorofare, NJ, 1992. [19] D. Sutherland, The development of mature gait, Gait Posture 6 (1997) 163–170, doi:http://dx.doi.org/10.1016/S0966-6362(97)00029-5.

W.-H. Hsu et al. / Gait & Posture 50 (2016) 75–81 [20] B. Vereijken, The complexity of childhood development: variability in perspective, Phys. Ther. 90 (2010) 1850–1859, doi:http://dx.doi.org/10.2522/ ptj.20100019. [21] L.G. Portney, M.P. Watkins, Foundations of Clinical Research: Applications to Practice, 3rd ed., Pearson/Prentice Hall, Upper Saddle River, N.J, 2009. [22] P. Meyns, L. Van Gestel, S.M. Bruijn, K. Desloovere, S.P. Swinnen, J. Duysens, Is interlimb coordination during walking preserved in children with cerebral palsy? Res. Dev. Disabil. 33 (2012) 1418–1428, doi:http://dx.doi.org/10.1016/j. ridd.2012.03.020. [23] P.G. Adamczyk, A.D. Kuo, Redirection of center-of-mass velocity during the step-to-step transition of human walking, J. Exp. Biol. 212 (2009) 2668–2678, doi:http://dx.doi.org/10.1242/jeb.027581. [24] N. Getchell, J. Whitall, How do children coordinate simultaneous upper and lower extremity tasks? The development of dual motor task coordination, J. Exp. Child Psychol. 85 (2003) 120–140, doi:http://dx.doi.org/10.1016/S00220965(03)00059-6.

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[25] J.S. Garciaguirre, K.E. Adolph, P.E. Shrout, Baby carriage: infants walking with loads, Child Dev. 78 (2007) 664–680, doi:http://dx.doi.org/10.1111/j.14678624.2007.01020.x. [26] R.W. Young, Evolution of the human hand: the role of throwing and clubbing, J. Anat. 202 (2003) 165–174, doi:http://dx.doi.org/10.1046/j.14697580.2003.00144.x. [27] G.W. Hewes, Food transport and the origin of hominid bipedalism, Am. Anthropol. 63 (1961) 687–710, doi:http://dx.doi.org/10.1525/ aa.1961.63.4.02a00020. [28] C.O. Lovejoy, The origin of man, Science 211 (1981) 341–350, doi:http://dx.doi. org/10.1126/science.211.4480.341. [29] C. Darwin, The Descent of Man, and Selection in Relation to Sex, John Murray, London, 1871. [30] A.R.E. Sinclair, M.D. Leakey, M. Norton-Griffiths, Migration and hominid bipedalism, Nature 324 (1986) 307–308, doi:http://dx.doi.org/10.1038/ 324307c0.