Report

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Research Report
䢇
The Relative Kicking Frequency of
Infants Born Full-term and Preterm
During Learning and Short-term and
Long-term Memory Periods of the
Mobile Paradigm
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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 (⬍33 weeks gestational age, ⬍2,500 g) and 10 comparison
infants participated in the study. Methods. The relative kicking frequencies of the tethered and nontethered legs were analyzed during
learning and short-term and long-term memory periods of the mobile
paradigm. Results. Infants born full-term showed an increase in the
relative kicking frequency of the tethered leg during the learning
period and the short-term memory period but not for the long-term
memory period. Infants born preterm did not show a change in
kicking pattern for learning or memory periods, and consistently
kicked both legs in relatively equal amounts. Discussion and Conclusion. Infants born full-term adapted their baseline kicking frequencies
in a task-specific manner to move the mobile and then retained this
adaptation for the short-term memory period. In contrast, infants born
preterm showed no adaptation, suggesting a lack of purposeful leg
control. This lack of control may reflect a general decrease in the
ability of infants born preterm to use their limb movements to interact
with their environment. As such, the mobile paradigm may be clinically
useful in the early assessment and intervention of infants born preterm
and at risk for future impairment. [Heathcock JC, Bhat AN, Lobo MA,
Galloway JC. The relative kicking frequency of infants born full-term
and preterm during learning and short-term and long-term memory
periods of the mobile paradigm. Phys Ther. 2005;85:8 –18.]
Key Words: Kicking, Motor control, Motor development, Motor learning, Premature infant.
8
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Jill C Heathcock, Anjana N Bhat, Michele A Lobo, James (Cole) Galloway
Physical Therapy . Volume 85 . Number 1 . January 2005
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I
nfants 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 oppor-
tunity 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,
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 preterm; 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.
Physical Therapy . Volume 85 . Number 1 . January 2005
Heathcock et al . 9
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 fullterm.18 Droit and colleagues20 found no difference in
* 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.
10 . Heathcock et al
Figure 1.
Home setup of mobile paradigm.
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
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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, researchers26 –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 ⬍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
Physical Therapy . Volume 85 . Number 1 . January 2005
Table 1.
Group Characteristics
Group
(nⴝ10)
Full-term
Comparison
Preterm
Age at Initial
Visit (d)
Sex
Male
Female
X
SD
3
5
9
7
5
1
106.6
109.3
103.6
9.9
14.5
13.9
Table 2.
Preterm Group Characteristics
X
SD
Range
Gestational
Age (wk)
Birth
Weight (g)
30.1
2.8
26–33
1,456
515
595–2,181
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 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
Heathcock et al . 11
Table 3.
Previously Unpublished/Unknown Characteristics of Preterm Group Infants in Neonatal Intensive Care Unit (NICU)a
Individual
Infant
Imaginga
1
2
3
4
5
6
7
8
9
10
X
SD
Range
a
N
N
Y
N
N
Y
Y
Y
Imaging Result
Suspect hydrocephaly, negative
PVL
IVH grade III
IVH grade I
Length of Time
in NICU (d)
Length of
Time on
Oxygen (d)
Diagnosis at 2–3 y
10
10
60
42
42
14
0
0
90
25
25
0
Gross motor delay
None
Speech delay
None
None
Developmental delay
17
36
28.87
18.67
10–60
9
4
19.13
30.52
0–90
Developmental delay
Hypotonia
N⫽no, Y⫽yes, PVL⫽periventricular leukomalacia, IVH⫽intraventricular hemorrhage. Data not available for infants 7 and 8.
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.
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 ⬍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
Testing Sessions
Infants in the full-term and comparison groups were
seen for 3 sessions, on 2 consecutive days and then 1
12 . Heathcock et al
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Figure 2.
Relative kicking frequency of full-term and comparison group infants across all sessions. Red box represents 45%–55%, or relatively equal kicking
rate of the right and left legs.
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
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
Physical Therapy . Volume 85 . Number 1 . January 2005
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
Heathcock et al . 13
Figure 3.
Relative kicking frequency of individual infants in the full-term and comparison groups during day 1 (learning). A value of ⬎1 (horizontal line)
represents a higher kicking rate with the right leg.
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).
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
14 . Heathcock et al
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
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Figure 4.
Relative kicking frequency of preterm group infants across all sessions. Red box represents 45% to 55%, or relatively equal kicking rates of the right
and left legs.
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
Physical Therapy . Volume 85 . Number 1 . January 2005
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
Heathcock et al . 15
Figure 5.
Relative kicking frequency of individual infants in the full-term and comparison groups during day 2 (short-term memory). A value of ⬎1 (horizontal
line) represents a higher kicking rate with the right leg.
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
16 . Heathcock et al
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
Physical Therapy . Volume 85 . Number 1 . January 2005
ўўўўўўўўўўўўўўўўўўўўўў
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 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 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.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
Physical Therapy . Volume 85 . Number 1 . January 2005
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
Heathcock et al . 17
clinical assessment tool as well as the performance of
infants born preterm at higher risk for future impairments.
17 Thelen E. Developmental origins of motor coordination: leg movements in human infants. Dev Psychobiol. 1985;18:1–22.
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