Periventricular leukomalacia

Background and Purpose. Infants born preterm differ in their spontaneous kicking, as well as their learning and memory abilities in the mobile paradigm, compared with infants born full-term. In the mobile paradigm, a supine infant's ankle is tethered to a mobile so that leg kicks cause a proportional amount of mobile movement. The purpose of this study was to investigate the relative kicking frequency of the tethered (right) and nontethered (left) legs in these 2 groups of infants. Subjects. Ten infants born full-term and 10 infants born preterm (

Key Words: Kicking, Motor control, Motor development, Motor learning, Premature infant.

Infants display spontaneous movements, that is, body movements without an external stimulus, beginning in utero and continuing throughout the first months of postnatal life.1 Historically, such movements of young infants have been viewed as reflexive and random. Although potentially useful for detecting nervous system impairments,2,3 these movements were not believed to have a major role in the development of purposeful motor behaviors. More recently, researchers4-6 have suggested that movements in early infancy have an important exploratory role in motor learning and motor skill acquisition. Early arm and leg movements, for example, provide infants with the opportunity to learn about the properties of their bodies,7 properties of their environments,8 and the match between them.8,9 Experience-dependent developmental plasticity has been identified in multiple neural systems, which suggest motor behaviors during early infancy are important for early brain development.10-12

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.18,17 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 colleagues10 noted differences in the kicking frequency of infants born at 30 weeks gestational age.19 Newborn infants born at

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

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.

Recently, researchers20-28 have used the mobile paradigm to investigate the ability of infants born full-term to adapt their spontaneous kicking pattern to cause mobile movement. In the simplest design, one limb is tethered to the mobile so that movement of the tethered leg causes a proportional amount of mobile movement.29 For example, 3-month-old infants increased the frequency of kicking a leg when it is tethered to the mobile, compared with when the same leg was not tethered.30 In a more complex design, infants learned to move the mobile by kicking with a specific range of knee flexion. Thus, young infants born full-term have the ability to cause mobile movement by adapting both general and specific features of their spontaneous kicking movements.

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

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 longterm memory periods, similar to the comparison group.

Methods

Participants

A total of 30 infants aged 3 to 4 months participated in the study. Infants were excluded from participation for any known visual or orthopedic diagnosis. Ten infants were in each of 3 groups: full-term, comparison, and preterm (Tab. 1). As reported earlier, the initial visit, the infants' ages, and gross motor skills did not differ. Detailed information on selection criteria, group assignment, and the infants' characteristics is provided in our previous report.31 A summary of characteristics of the infants born preterm is shown in Table 2. Table 3 shows the available medical history and follow-up information from 8 of the 10 infants born preterm. The infants born preterm spent an average of 28.87 days (SD = 18.27) in the neonatal intensive care unit and an average of 19.13 days (SD = 30.52) on oxygen. Four of the 8 infants did not have imaging tests at birth, 1 infant was diagnosed with periventricular leukomalacia, and 2 infants were diagnosed with intraventricular hemorrhage. Infants were admitted into the study following informed parental consent as approved by the University of Delaware Human Subjects Review Committee and Christiana Care Hospital Institutional Review Board.

Apparatus

Two identical white plastic mobile stands were attached to the right and left sides of the infants' home cribs (Fig. 1). A white ribbon and a small, soft cuff were used to tether each infant's right leg to the right stand.31

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)] × 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

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

Results

Relative Frequency During the Learning Period

Infants born full-term showed an increase in the relative kicking frequency of the tethered leg over one 15-minute session. 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 52.16% to 66.56%. A majority (14/15) of relative kicking frequency percentages for each time period were above 55%, suggesting that infants in the full-term group kicked the tethered leg more than the nontethered leg. The standard deviations were high, ranging from 4.27% to 15.67%.

During baseline day 1, the infants born full-term had a mean of 6.06 (SD = 6.4) tethered leg kicks and 5.5 (SD=4.3) nontethered leg kicks, resulting in a ratio value of 52% (SD = 10.6%) (Fig. 2). Within the first 3 minutes of acquisition day 1, infants born full-term began kicking their tethered leg. The first purpose of the present study was to determine how infants adapt the baseline kicking frequencies of both legs to meet task demands of their tethered leg more than their nontethered leg, as reflected in a relative kicking frequency of 62% (SD = 12.7%). Full-term group infants kicked more frequently with their tethered leg throughout all other acquisition periods and during extinction of day 1, with a peak of 66% (SD = 9.8%) during acquisition 02 (Fig. 2). A repeated-measures ANOVA showed a difference in the ratio for time period (F=3.73; df=4,36; P=.01). Planned comparisons showed increases in the relative kicking frequency between baseline and acquisition 02 (P=.006) and baseline and extinction (P=.01).

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 1 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).

In contrast to infants born full-term, infants born preterm did not show an increase in relative kicking frequency at any point during the 6 weeks of testing. The relative kicking frequency (Fig. 4) across all time periods (baseline, acquisition 01, acquisition 02, acquisition 03, and extinction) for each of the 12 testing sessions ranged from 43.62% on week 1 day 2 to 62.57% on week 3 day 2. A majority (56/60) of relative kicking frequency percentages for each time period were between 45% and 55%, suggesting that infants in the preterm group kicked their tethered and nontethered legs in equal amounts. The standard deviations were high, ranging from 4.32% on week 4 day 1 to 17.46% on week 3 day 2. As reported previously,31 infants in the preterm group had increased the normalized kicking frequencies of their tethered leg in comparison with their own baseline level on week 1 day 1, week 2 day 1, and week 4 day 1. Thus, the relative kicking frequency was statistically analyzed during these periods. During baseline day 1, the preterm group's relative kicking frequency was 50.3% (SD = 12.5%), which was not different from that of infants in the full-term or comparison groups (P=.70 and P=.21, respectively). There was no effect for time period for the preterm group's relative kicking frequency during day 1 as measured with an ANOVA (F=1.472; df=4,36;P=.23).

No differences in relative kicking frequency were found between the preterm and comparison groups during any acquisition or extinction period on day 1 (P=.72, P=.73, P=.73, and P=.61, respectively). Five of the 10 infants born preterm showed an increase in relative kicking frequency during extinction as compared with baseline on day 1.

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.

The preterm group did not display short-term and long-term memory over the 6 weeks of testing.31 Their relative kicking frequency remained between 45% and 55% during all baseline periods for all weeks (Fig. 4). Their kicking did not differ between the baseline periods between any 2 weeks of testing. On an individual level, 4 to 6 infants born preterm showed an increase in the relative kicking frequency from baseline day 1 to baseline of any other weeks.

Discussion and Conclusions

Our hypotheses regarding the relative kicking frequencies of the full-term group and the preterm group during the learning and memory periods in the mobile paradigm were supported with one exception. As predicted, infants born full-term were able to independently learn a task-specific pattern of kicking within the first 15-minute session and retain that pattern for 24 hours. Unexpectedly, infants born full-term did not retain this pattern for 1 week. Also as expected, infants born preterm displayed a relatively equal kicking frequency of their tethered and nontethered legs during all 12 sessions across the 6 weeks.

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 bom fullterm 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 neuromptor 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 lirst few months of life. By 3 months of age, infants will produce specific intralimb and interlimb patterns required to move a mobile.26-28,34 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 extension-a pattern not common in this age group-when 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 fullterm 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.

* 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.

References

1 Groome LJ, Swiber MJ, Holland SB, et al. Spontaneous motor activity in the perinatal infant before and after birth: stability in individual differences. Dev Psychobiol. 1999;35:15-24.

2 Prechtl HF. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23:151-158.

3 Kravitz H, Boehm JJ. Rhythmic habit patterns in infancy: their sequence, age of onset, and frequency. Child Dev. 1971;42:399-413.

4 Pick JP, Carman R. Developmental profiles of spontaneous movements in infants. Early Hum Dev. 1994;39:109-126.

5 Thelen E, Bradshaw G, Ward JA. Spontaneous kicking in month-old infants: manifestation of a human central locomotor program. Behav Neural Biol. 1981;32:45-53.

6 Lobo MA, Galloway JC, Savclsbergh GJP. General and task-related experiences affect early object interaction. Child Dev. 2004;75: 1268-1281.

7 Turvey MT, Fitzpatrick P. Commentary: development of perceptionaction systems and general principles of pattern formation. Child Dev. 1993;64:1175-1190.

8 Kawai M, Savelsbergh GJP, Wimmers RH. Newborns' spontaneous arm movements are influenced by the environment. Early Hum Dev. 1999;54:15-27.

9 Thelen E, Corbetta D, Kamm K, et al. The transition to reaching: mapping intention and intrinsic dynamics. Child Dev. 1993;64: 1058-1098.

10 Martin JH, Choy M, Pullman S, Meng Z. Corticospinal system development depends on motor experience. J Neurosci. 2004;24: 2122-2132.

11 Berardi N, Pizzorusso T, Maffei L. Critical periods during sensory development. Curr Opin Neurobiol. 2000;10:138-145.

12 Inglis FM, Zuckerman KE, Kalb RG. Experience-dependent development of spinal motor neurons. Neuron. 2000;26:299-305.

13 Thelen E, Ridley-Johnson R, Fisher D. Shifting patterns of bilateral coordination and lateral dominance in the leg movements of young infants. Dev Psychobiol. 1983;16:29-46.

14 Vaal J, van Soest AJ, Hopkins B. Spontaneous kicking behavior in infants: age-related effects of unilateral weighting. Dev Psychobiol. 2000;36:111-122.

15 Thelen E, Fisher DM. From spontaneous to instrumental behavior: kinematic analysis of movement changes during very early learning. Child Dev. 1983;54:129-140.

16 Geerdink JJ, Hopkins B, Beek WJ, Heriza CB. The organization of leg movements in preterm and full-term infants after term age. Dev Psychobiol. 1996;29:335-51.

17 Thelen E. Developmental origins of motor coordination: leg movements in human infants. Dev Psychobiol. 1985;18:1-22.

18 Pick JP, Gasson N. Spontaneous kicking in full-term and preterm infants: are there leg asymmetries? Hum Mov Sci. 1999;18:377-395.

19 Jeng SF, Chen LO, Yau KI. Kinematic analysis of kicking movements in preterm infants with very low birth weight and full-term infants. Phys Ther. 2002;82:148-159.

20 Droit S, Boldrini A, Cioni G. Rhythmical leg movements in low-risk and brain-damaged preterm infants. Early Hum Dev. 1996;44:201-213.

21 Vaal J, van Soest AJ, Hopkins B, et al. Development of spontaneous leg movements in infants with and without pcrivcntricular leukomalacia. Exp Brain Res. 2000;135:94-105.

22 Piek JP. The influence of preterm birth on early motor development. In: Piek JP, ed. Motor Behavior and Human Skill: A Multidisciplinary Approach. Champaign, Ill: Human Kinetics Inc; 1998;233-252.

23 Galloway JC, Thelen E. Feet First: object exploration in young infants. Infant Behavior and Development. 2004;27:107-112.

24 Rovee-Collier CK, Hayne H, Colombo M. The Development of Implicit and Explicit Memory. Vol 24. Philadelphia, Pa: John Benjamins Publishing Co; 2001:322. Series B: Research in Progress-Experimental, Descriptive, and Clinical Research in Consciousness.

25 Sullivan MW, Rovee-Collier CK, Tynes DM. A conditioning analysis of infant long-term memory. Child Dev. 1979;50:152-162.

26 Chen Y-P, Fetters L, Holt KG, Saltzman E. Making the mobile move: constraining task and environment. Infant Behavior and Development. 2002;25:195-220.

27 Angulo-Kinzler RM. Exploration and selection of intralimb coordination patterns in 3-month-old infants. J Mot Behav. 2001;33:363-376.

28 Angulo-Kinzler RM, Ulrich B, Thelen E. Three-month-old infants can select specific leg motor solutions. Motor Control. 2002;6:52-68.

29 Rovee CK, Rovee DT. Conjugate reinforcement of infant exploratory behavior. J Child Psychol. 1969;8:33-39.

30 Rovee-Collier CK, Morrongiello BA, Aron M, Kupersmidt J. Topographical response differentiation and reversal in 3-month-old infants. Infant Behavior and Development. 1978;1:323-333.

31 Heathcock JC, Bhat AN, Lobo MA, Galloway JC. The performance of infants born preterm and full-term in the mobile paradigm: learning and memory. Phys Ther. 2004;84:808-821.

32 Gekoski MJ, Fagen JW, Pearlman MA. Early learning and memory in the preterm infant. Infant Behavior and Development. 1984;7:267-276.

33 Thelen E, Smith LB. A Dynamic Systems Approach to the Development of Cognition and Action. Cambridge, Mass: MIT Press; 1993:414. Bradford Books Scries in Cognitive Psychology.

34 Thelen E. Three-month-old infants can learn task specific patterns of interlimb coordination. Psychol Sci. 1994;5:280-285.

35 Jeng SF, Chen LC, Tsou KI, et al. Relationship between spontaneous kicking and age of walking attainment in preterm infants with very low birth weight and full-term infants. Phys Ther. 2004;84:159-172.

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@udel.edu).

All authors provided concept/idea/research design and consultation (including review of manuscript before submission). Ms Heathcock and Dr Galloway provided writing. Ms Heathcock, Ms Bhat, and Ms Lobo provided data collection, and Ms Heathcock provided data analysis. Ms Heathcock, Dr Galloway, and Ms Bhat provided project management. Dr Galloway provided facilities/equipment and institutional liaisons. The authors thank the families involved in the study for their participation. They also thank Kathleen H Leef, RN, MSN, and David A Paul, MD, for their assistance with recruiting infants born prcterm; Dr John Scholz and Dr Lynn Snyder-Mackler for their helpful comments; and Robert Cardillo for his assistance with programming.

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 5-7, 2003, Savannah, Ga, and at the annual International Conference on Infant Studies, May 5-8, 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.

This article was received November 6, 2003, and was accepted April 15, 2004.

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