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Research Reports |
JC Heathcock, PT, MPT, is Physical Therapist, Department of Physical Therapy, University of Delaware, Newark, Del, and a doctoral student in the Biomechanics and Movement Science Program, Department of Biomechanics and Movement Science, University of Delaware. This study was conducted in partial fulfillment of the requirements for Ms Heathcock's master's thesis at the University of Delaware
AN Bhat, PT, MSc, is Physical Therapist, Department of Physical Therapy, and a doctoral student in the Biomechanics and Movement Science Program, Department of Biomechanics and Movement Science, University of Delaware
MA Lobo, PT, MPT, is Physical Therapist, Department of Physical Therapy, and a doctoral student in the Biomechanics and Movement Science Program, Department of Biomechanics and Movement Science, University of Delaware
JC Galloway, PT, PhD, is Physical Therapist and Assistant Professor, Department of Physical Therapy and Biomechanics and Movement Science Program, University of Delaware
Address all correspondence to Dr Galloway at University of Delaware, 301 McKinly Lab, Newark, DE 19716 (USA) (jacgallo{at}udel.edu)
Submitted November 6, 2003;
Accepted April 15, 2004
| Abstract |
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Key Words: Kicking Motor control Motor development Motor learning Premature infant
| Introduction |
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Leg movements in infants born full-term have frequently been studied. Awake, active infants kick from 4 to 80 times per minute,4,13 with the peak kicking frequency noted during the first months of life.14,15 Infants born full-term change their kicking frequency and kicking patterns over the first 12 months of life. For example, these infants decrease their kicking frequency14,16 and change the pattern of motion of the hip, knee, and ankle of a single leg (intralimb) and pattern of motion between limbs (interlimb).
Newborn infants born full-term will flex and extend their hips, knees, and ankles so that the timing is similar between joints, which is termed "coupling." Newborns most frequently produce alternating kicks, in which a kick with one leg is likely to be followed by a kick with the opposite leg.13,17 From 1 to 4 months of age, infants born full-term increase the percentage of single-leg kicks.13 At 2 months of age, the coupling between hip and ankle motion of one leg begins to decrease.17 Individual infants may display a preference for kicking one leg over the other5,13; however, as a group, infants 6 through 26 weeks of age kick with relatively equal frequency between the right and left legs.14 By 5 to 6 months of age, infants kick with a greater variety of interlimb patterns as compared with younger infants18; however, a bilaterally symmetrical pattern, in which both legs flex and extend at relatively the same time, is the most common pattern.13 By 10 months of age, infants kick with interlimb coupling; however, the joints move in opposite directions, such as knee flexion with hip extension.17 Thus, over the first year of life, spontaneous kicking becomes more flexible, complex, and variable within as well as between the legs.17
Infants born preterm display different kicking frequencies and kicking patterns than infants born full-term. Geerdink and colleagues16 noted differences in the kicking frequency of infants born at <32 weeks gestational age compared with infants born full-term during certain periods of development. At 6 weeks of age,* infants born preterm had a higher kicking frequency than infants born full-term, but by 12 weeks of age, the differences were no longer statistically significant.16 At 2 to 4 months of age, infants born at <30 weeks gestational age and with very low birth weight had a higher kicking frequency than infants born full-term and infants born at >30 weeks gestational age.19 Newborn infants born at <32 weeks gestational age showed greater hip-ankle and knee-ankle coupling than infants born full-term.16 Other researchers have found a similar increase in hip-ankle coupling in the right leg of infants born preterm and at low risk for future impairments as well as little or no decrease in intralimb coupling with age as is seen in infants born full-term. Furthermore, these infants born preterm show greater differences between the right and left legs than infants born full-term.18 Droit and colleagues20 found no difference in kicking frequency of newborn infants born preterm who were at low risk for future impairments and those with known brain damage at 31 to 35 weeks and 35 to 39 weeks postmenstrual age. Infants born preterm with periventricular leukomalacia showed a different developmental course of kicking from 6 to 26 weeks of age compared with infants born full-term, including an inability to disassociate intralimb coupling.21
Infants born preterm also kick with interlimb features that differ from those of infants born full-term. For example, newborn infants with brain damage produce a higher frequency of in-phase kicks, where both legs kick at the same time, than infants born preterm who are at lower risk for future impairments.20 At 2 to 4 months of age, infants born preterm born at <30 weeks gestational age with very low birth weight showed higher interlimb correlation and lower variability of interlimb kicking patterns than infants born full-term.19 Infants born preterm, for example, displayed more coupling between legs than infants born full-term, suggesting an inability to dissociate the 2 legs during kicking.19 Persistent coupling of the legs has been proposed to hinder the development of purposeful control.22
Infants born full-term and without known disease begin to gain purposeful control of their legs within the first months of postnatal life.23 In a now-classic series of studies, Rovee-Collier and colleagues24 developed an associative learning paradigm to study the ability of young infants to learn and remember a cause-and-effect relationship between movement of their body and movement of their immediate environment. In the "mobile paradigm," infants were placed supine in their cribs with one leg tethered to an overhead mobile (Fig. 1). Infants as young as 8 weeks of age learned the association between leg and mobile movement, in that they increased the frequency of kicking to move the mobile within one 15-minute session and remembered the association for up to 1 week.25 By taking advantage of infants' early leg kicking, these researchers demonstrated young infants' basic learning and memory abilities.
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In our recent work with infants born full-term,31 we showed that infants born full-term learned the association between kicking and mobile movement. Specifically, they increased their kicking rate as compared with their own baseline kicking rate and with a comparison group who saw a moving mobile but whose tethered leg did not cause mobile movement. The infants born full-term showed an increased kicking rate within one session (learning period) and retained an elevated rate for 24 hours (short-term memory period) and for 1 week (long-term memory period). Because only the right leg was tethered to the mobile, the task required only that infants kick the right leg to move the mobile. The first purpose of the present study was to determine how infants adapt the baseline kicking frequencies of both legs to meet task demands. Given that the infants born full-term rapidly learned the associative learning aspect of the paradigm and that they displayed the ability to dissociate their legs during spontaneous kicking, we hypothesized that infants born full-term would preferentially increase the kicking frequency of the tethered leg during the learning period and maintain this pattern during both the short-term and long-term memory periods.
Several studies have examined the spontaneous kicking of infants born preterm; however, very few studies have examined their kicking in a task-specific manner such as within the mobile paradigm.32 Gekoski and colleagues32 showed that infants born preterm and at low risk for future impairments with a gestational age of <36 weeks took an extra session to learn the paradigm and did not show long-term memory. Recently, we showed that 3- to 4-month-old infants born preterm (birth weight <2,500 g and gestational age <33 weeks) did not display learning despite having 12 sessions over 6 weeks.31 These infants, however, did increase their tethered leg kicking frequency compared with their baseline kicking frequency during certain sessions but never greater than the comparison group.31
Thus, the second purpose of the present study was to determine whether this increase in tethered kicking frequency was specific to the tethered leg, as predicted for the infants born full-term, or was simply a general increase in the kicking frequency of both legs. Given that these infants born preterm31 displayed neither associative learning in the mobile paradigm nor the typical ability to dissociate their leg kicks during spontaneous kicking, we hypothesized that they would not preferentially increase the kicking frequency of the tethered leg during the learning period but would equally increase the kicking frequency of both legs. Moreover, we hypothesized that they would maintain a relatively equal kicking frequency with both legs during the short-term and long-term memory periods, similar to the comparison group.
| Methods |
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Procedure
Testing sessions were completed in the infants in their home cribs. Each infant was placed in a supine position by a parent who then remained out of the infant's sight. For the first 3 minutes, termed "baseline," the mobile was attached to the left stand; when the infant kicked, the mobile did not move. For the next 9 minutes, termed "acquisition," the mobile was switched to the right stand for the infants born full-term and preterm so that tethered leg kicks resulted in a proportional amount of mobile movement. For the comparison group, the mobile remained on the left stand while an investigator, who remained out of the infants' view, used a transparent wire to move the mobile. During minutes 12 to 15, termed "extinction," the mobile was on the left stand for all groups so that kicking did not move the mobile.
Testing Sessions
Infants in the full-term and comparison groups were seen for 3 sessions, on 2 consecutive days and then 1 week later. Using a normalized kicking frequency, the infants in the full-term group displayed learning on day 1, short-term memory 24 hours later on day 2, and long-term memory 1 week later on day 3.31 The normalized kicking frequency is the kicking frequency for each acquisition and extinction period divided by the infant's baseline kicking frequency. The comparison group did not increase their kicking during learning or memory period. Infants in the preterm group were seen for 2 consecutive days each week for 6 weeks.31 Infants born preterm did not display learning across any of the 12 testing sessions because they did not display an increase in their normalized kicking frequency as compared with the comparison group. The infants in the preterm group, however, did show an increase in kicking during certain acquisition or extinction period as compared with their own baseline for that day. Therefore, relative kicking frequency was analyzed during the time period when this increase was observed.
A kick was defined as a simultaneous extension of the hip and knee with immediate recoil of flexion. Tethered leg (right) and nontethered leg (left) kicks were counted during all time periods of each session. The percentage of total kicks by the tethered leg was calculated by the equation: [tethered leg kicks/(tethered leg kicks + nontethered leg kicks)] x 100. This value was termed the "relative kicking frequency." A relative kicking frequency score of 50% indicates that both legs kicked equal amounts, whereas a frequency score of <50% indicates the tethered leg kicked more often. Intrarater and interrater reliability for kicking frequency were .95 using a 2-way mixed-effects intraclass correlation coefficient.31
Data Analysis
To test whether infants kicked differently during acquisition and extinction as compared with baseline, relative kicking frequency scores were compared within each group by separate repeated-measures analyses of variance (ANOVAs) across time periods of the same day, followed with planned comparisons between periods. To test whether infants retained the same or different kicking patterns in later sessions as they displayed during learning, relative kicking frequency scores were compared within each group by separate repeated-measures ANOVAs across the baseline periods of 2 days separated by 24 hours for short-term memory and across baseline periods separated by 1 week for long-term memory. The relative kicking frequencies for these baseline periods also were compared between the full-term and comparison groups and between the preterm and comparison groups with separate independent t tests. For all tests, values were considered significant at P<.05.
| Results |
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For the comparison group, the relative kicking frequency (Fig. 2) across all time periods (baseline, acquisition 01, acquisition 02, acquisition 03, and extinction) for each of the 3 testing sessions ranged from 42.10% to 57.33%. In addition, a majority (10/15) of relative kicking frequency percentages for each time period were between 45% and 55%, suggesting that infants in the comparison group kicked the tethered and nontethered legs in equal amounts. The standard deviations were high, varying from 6.89% to 22.30%. The full-term group proportionally increased their relative kicking frequency such that the tethered leg kicked more frequently as soon as kicking led to mobile movement (acquisition 01), whereas the comparison group, whose leg kicks did not cause mobile movement, did not show this change.
The full-term group also showed a difference in the relative kicking frequency compared with the comparison group. In the initial baseline period, before the mobile reinforced kicking, the relative kicking frequencies of infants in the full-term and comparison groups were approximately 50% and did not differ between groups (P=.2). Infants in the full-term group had greater relative kicking frequencies than the comparison group during acquisition 02 (P=.001) and extinction (P=.01) as measured by independent t tests. In addition to group differences, individual infants in the full-term and comparison groups differed. Eight of the 10 infants in the full-term group increased the relative kicking frequency during extinction compared with baseline. In contrast, only 3 of the 10 infants in the comparison group showed an increase (Fig. 3).
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For week 2 day 1, there were no statistically significant differences in relative kicking frequency among the time periods (F=1.145; df=4,36; P=.35). For week 4 day 1, there also were no differences across among the time periods (F=0.844; df=4,36; P=.50). Planned comparisons between baseline and acquisition 01, acquisition 02, and acquisition 03 for week 2 day 1 and week 4 day 1 were not significant. Additionally, there were no differences in relative kicking frequency between the preterm group and the comparison group. On an individual level, 4 to 6 infants born preterm showed an increase in relative kicking frequency from baseline to extinction during any given week.
Relative Kicking Frequency During the Short-term and Long-term Memory Period
Infants in the full-term group maintained an increase in relative kicking frequency for the short-term memory period (24 hours later), but not for the long-term memory period (1 week later). The average relative kicking frequency increased from 52% (SD=3%) for the baseline measurement on day 1 to 64% (SD=4%) for the baseline measurement on day 2 and 62% (SD=4%) for the baseline measurement on day 3 (Fig. 2). The repeated-measures ANOVA showed a trend in relative kicking frequency across time period (F=2.691; df=2,18; P=.095). We continued with this analysis as the comparisons between the relative kicking frequency between baseline day 1 and day 2 (short-term memory) and the relative kicking frequency between baseline day 1 and day 3 (long-term memory) were planned. These planned comparisons showed an increase in relative kicking frequency between baseline day 1 and day 2 (P=.013), but not between baseline day 1 and day 3 (P=.17). Similarly, the full-term group also had greater relative kicking frequencies than the comparison group during baseline day 2 (P=.01), but not during baseline day 3 (P=.25), as measured by independent t tests.
Full-term and comparison groups differed at the level of individual infants. Eight of the 10 full-term group infants increased their relative kicking frequency during baseline day 2 compared with baseline day 1. In contrast, only 1 of the 10 infants in the comparison group showed an increase (Fig. 5). Although the groups did not differ during the long-term memory period, 6 of the 10 infants born full-term increased their relative kicking frequency during the long-term memory period, whereas no infants from the comparison group showed an increase.
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| Discussion and Conclusions |
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Our results extend those of a previous study in which infants born full-term increased movement in whichever limb was tethered to the mobile during a single session.30 First, our results suggest that infants born full-term can produce a task-specific kicking pattern as compared with a comparison group that was tethered, but did not have control of the mobile. Second, our results suggest that these infants can retain this task-specific pattern for 24 hours following the initial learning period. Although these infants displayed long-term memory for the initial associative learning, as evidenced by an increase in tethered leg kicks,31 they also increased nontethered leg kicks so that tethered and nontethered leg kicks were not statistically different than the pre-exposure relative kicking frequency. Taken together, our results suggest that, although infants born full-term retained the memory for the association between leg movement and mobile movement for up to 1 week, they retained the task-specific relative kicking frequency only for 24 hours.
In contrast, the preterm group displayed relative kicking frequencies after exposure to the mobile reinforcement that were not different from their baseline pattern on day 1 before any exposure to the mobile. Their relative kicking frequencies also did not differ from those of the infants in the comparison group. That is, the increase in tethered leg kicks by these infants31 was accompanied by an equal increase in kicking frequency of the nontethered leg (Fig. 3). This lack of a task-specific pattern was also noted at the level of individual infants in that equivalent numbers of infants born preterm showed a task-specific pattern and an equal kicking frequency between legs during each day of testing.
Developmental changes in motor behaviors have been proposed to emerge out of the social, cognitive, and perceptual-motor aspects of past experiences as well as the current context and task requirements.33 Infants likely gain knowledge about how their limbs move by daily experience kicking their legs.22 We correctly predicted the performance of the full-term and preterm groups' relative kicking frequencies during the mobile paradigm based on general features from studies of each group's spontaneous kicking. This suggests the potential for a relationship between spontaneous kicking patterns and those patterns used as infants perform in the mobile paradigm. Specifically, newborn infants born full-term kick with a stereotypically alternating pattern, which becomes more variable and includes frequent individual leg kicks over the next 6 months.4,13 The infants in our study who were born full-term may have taken advantage of the experience of single-leg kicking during their spontaneous kicking when the opportunity arose to increase the kicking frequency of a single leg to control the mobile. In contrast, infants born preterm spontaneously kick with a higher interlimb correlation and display fewer interlimb kick patterns than infants born full-term.18,19 As a result, the infants in our study who were born preterm may not have had enough experience kicking with a single leg to be able to preferentially increase the kicking frequency of a single leg to move the mobile.
Infants born preterm differed from infants born full-term in their ability to produce task-specific leg movements during a task in which leg movements were directly associated with mobile movement. This suggests a potentially important connection between associative learning and neuromotor control during early infancy. That is, the inability of these infants to disassociate their leg movements may have affected their ability to learn the basic association between leg movement and mobile movement. Alternatively, if these infants were unable to rapidly learn the association between leg and mobile movement, then mobile movement may have caused an increase in kicking simply via arousal. That is, it is possible that infants born preterm may not have shown a task-specific kicking pattern because they may not have realized that the mobile could be manipulated via kicking.
Our results join those of several recent studies to provide converging evidence that infants born full-term display purposeful leg control during the first few months of life. By 3 months of age, infants will produce specific intralimb and interlimb patterns required to move a mobile.2628,34 In addition to the task-specific pattern shown in our study, young infants born full-term appear to be able to selectively increase the frequency of specific movement patterns, including those rarely seen until later infancy. For example, 3- to 4-month-old infants changed their bilateral kicking after experiencing the mobile paradigm setup where both legs were tethered together (both legs extend and flex simultaneously), and remembered this pattern for 24 hours.34 Recently, the manipulations of the mobile paradigm have become more complex. Three-month-old infants chose to kick within a specific knee range of motion when this range of motion caused mobile movement.27 In addition, 4-month-old infants increased the frequency of leg movements involving hip flexion and knee extensiona pattern not common in this age groupwhen this pattern caused mobile movement.28 It is not known how long infants born full-term are able to retain these patterns. Most recently, Galloway and Thelen23 showed that infants 2 to 4 months of age were able to control their legs to repeatedly place their feet on objects. This "feet reaching" occurred, on average, 4 weeks before the infants could reach for the same objects with their hands.23 In summary, it appears that infants born full-term display purposeful limb control much earlier than traditionally thought.
The inability of young infants born preterm to adapt their leg movements to task requirements may suggest an early impairment in leg control, which in turn may hinder the development of later skills.22 For example, recent work suggested a link between early spontaneous kicking in infants born preterm and later delays in locomotion.35 It is important to note that the long-term impact of the kicking frequency displayed by infants born preterm in this study is not known. Additional studies are necessary to determine the predictive capacity of infants' performance in the mobile paradigm.
The mobile paradigm is a potentially useful clinical tool for information regarding leg control in combination with associative learning and memory in young infants. In addition, future studies can build on the findings of the present study to investigate the effect of training on the ability of infants born preterm to adapt other aspects of their kicking patterns that they may be able to control during the periods of learning and short-term and long-term memory. The mobile paradigm provides information in a relatively short time using a low-tech, inexpensive protocol that allows assessment within the home or clinic.
It is important to note that this was the first study of the relative kicking frequency changes seen in the mobile paradigm in infants born full-term and those born preterm. Thus, there are several limitations to the interpretation of these results. First, the design was imbalanced because the preterm group was seen for 6 weeks, whereas the full-term and comparison groups were seen for 1 week. Although kicking frequencies during the baseline period remained relatively stable across the 12 visits of the infants born preterm, it is not known how the full-term or comparison groups might have performed over 6 weeks. Infants born preterm kicked with a consistently equal frequency over the 6-week period; however, this finding does not mean that their kicks remained identical over that period. Second, we measured only changes in kicking frequency and not patterns of movement. Several other features describing alternating, unilateral, and bilateral kicking patterns that were not measured that may have changed during the mobile paradigm. Changes in kicking patterns not measured may signify learning of the mobile paradigm. Studies are necessary to determine the merits of the mobile paradigm as a clinical assessment tool as well as the performance of infants born preterm at higher risk for future impairments.
| Footnotes |
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This study was approved by the University of Delaware Human Subjects Review Committee and the Christiana Care Institutional Review Board.
This research was presented, in part, as poster presentations at the annual North American Society for the Psychology of Sport and Physical Activity, June 57, 2003, Savannah, Ga, and at the annual International Conference on Infant Studies, May 58, 2004, Chicago, Ill.
This work was partly funded by Foundation for Physical Therapy PODS I awards to Ms Heathcock and by a University of Delaware Research Foundation award to Dr Galloway.
* Ages of infants born preterm are reported as "age adjusted," calculated from the actual birth date versus from the expected due date unless specified differently. ![]()
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