- Email: [email protected]
The use of somatosensory information during the acquisition of independent upright stance
THE USE OF SOMATOSENSORY INFORMATION DURING THE ACQUISITION OF INDEPENDENT UPRIGHT STANCE los~ A. Barela University of Maryland and Universidade Estadual Paulista
John I. leka Jane E. Clark University of Maryland
This study investigated developmental changes in the use of a contact surface during the acquisition of upright posture. Standing infants were longitudinally examined at four developmental epochs: pulling to stand (PS); standing alone (SA); walking onset (WO); and 1.5 months post-walking (PW). The results revealed that as standing experience increased the force applied to the contact surface by the hand and the body sway decreased. Applied force and body sway were consistently related in the anterior-posterior direction (r ~, 0.65). Temporally, body sway led applied force ( - 45ms) at the PS, SA, and WO developmental periods. However, at PW, the temporal relationship reversed and applied force led body sway (~ 140 ms). These results indicate that initially infants use surface contact for mechanical purposes but later for orientation information that affords prospective control of posture.
posture development somatosensory prospective infancy
The acquisition of independent upright stance constitutes a major challenge for young infants to solve. Indeed it is not until around the age of 8 months that infants pull themselves to a stand and near 11 months when they stand independently (Capute, Shapiro, Palmer, Ross, & Wachtel, 1985; Frankenburg, Dodds, Archer,
Shapiro, & Bresnick, 1992). As infants struggle to find a solution to the puzzle of how to stand, they discover that their surrounding environment provides support for their newly emerging posture. For example, before they stand upright independently, infants are often observed using a couch or table for assistance.
• Jane E. Clark, University of Maryland, Department of Kinesiology, College Park, MD, 20741-2611; e-mail: [email protected]. INFANT BEHAVIOR & DEVELOPMENT22 (1), 1999, pp. 87-102 Copyright © 1999 Elsevier Science Inc.
ISSN 0163-6383 All rights of reproduction in any form reserved.
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
In the present paper, we investigate this use of surface contact as infants progress in their ability to stand independently. Our hypothesis is that surface contact initially provides mechanical support, but then becomes a source of sensory information for upright stance orientation that affords anticipatory or prospective control of posture. The postural control system receives information about the body and its environment from three sensory systems: visual, vestibular and somatosensory (Nashner, 1981). Of the three sensory inputs, the visual system has received the most attention in the development of infant postural control (see Bertenthal & Clifton, 1998, for a review). The few developmental studies investigating the role of the vestibular and somatosensory systems have shown well-organized postural responses in the absence of vision. For example, Woollacott, Debfi, and Mowatt (1987) demonstrated that 4-month-olds and older infants with their eyes covered with opaque goggles consistently and correctly activated the appropriate muscles in response to platform perturbations. Moreover, 12- to 14-month-olds are capable of maintaining upright stance in the dark (Ashmead & McCarty, 1991). In both studies, infants performed better when vision was absent, suggesting an important role for somatosensory and vestibular inputs in infants' postural development. The small number of studies on the role of somatosensory and vestibular inputs in infant postural control represents a gap in the infant sensorimotor literature that deserves attention. Part of the reason for this gap may be the difficulty in devising experimental situations that enable postural development in infants to be analyzed. Typically postural tasks require standing quietly for 20-30 seconds. Obviously this is an impossible task for the infant struggling to learn upright postural control. Once quiet standing is achieved, the developmental process may have passed. However recent work by Jeka and Lackner (Holden, Ventura, & Lackner, 1994; Jeka & Lackner, 1994, 1995) suggests an experimental paradigm that
may offer a window into the role of somatosensory information for infant postural development. In these experiments, body sway was significantly attenuated when subjects touched a stationary surface with the right index fingertip. Over 60% of body sway attenuation occurred not only when the fingertip provided mechanical support (5-8 N), but also when force levels were too small (< 1 N) to provide mechanical support of body sway (Holden, Ventura, & Lackner, 1994; Jeka & Lackner, 1994). In both situations, body sway and applied force were spatially correlated, meaning that as the subject swayed toward the contact surface, the applied force increased in that direction and vice versa. However, the temporal relationship between body sway and applied force differed depending on the level of applied force. In the condition in which subjects were allowed to apply as much force as desired (high force), changes in applied force led body sway by less than 100 ms. In the light touch condition (< 1 N of applied force), changes in applied force led body sway by 200-300 ms (Jeka & Lackner, 1994). Further investigation showed appropriate anticipatory postural muscle activity within the 200-300 ms period between changes in force application and body sway (Jeka & Lackner, 1995). Jeka and Lackner (1995) concluded that subjects were extremely sensitive to small force changes at the fingertip and that these changes provide sensory cues used to attenuate body sway through appropriate postural muscle activation. In essence, force changes at the fingertip provide a model of body sway that adults use to activate postural muscles in an anticipatory or feedforward fashion, resulting in attenuated sway. These adult findings offer several implications for postural development in infants. First, the intuitive notion is that infants are deriving mechanical support for the body from contact with a rigid surface (e.g., a coffee table). But this may be true only at the earliest stages of upright support. Another form of 'support' may be the somatosensory information obtained from fingertip and hand contact. Sec-
The Use of Somatosensory Information
ond, the temporal relationship between body sway and contact forces at the hand may signal the onset of prospective control of posture with infants. If infants change their use of the surface contact from mechanical to informational support, then we should expect a similar change in the temporal relationship between applied force and body sway as observed in Jeka and Lackner (1994). Although prospective control has been demonstrated in infants' reaching tasks (von Hofsten, 1983) and in visual pursuit (e.g., von Hofsten & Rosander, 1996, 1997), there is no evidence that prospective or feedforward control is achieved in infants standing upright before they can walk, when walking emerges or after a few months of walking experience. Clearly, feedforward or anticipatory muscle activity provides an important strategy for the postural control system (Houk & Lehman, 1987). Belenkii, Gurfinkel, and Paltsev (1967) illustrated this concept with a simple task of raising the right arm from the hip to a horizontal position at shoulder height while standing. Recordings of EMG activity showed that prior to activity in the right shoulder and arm, a burst of EMG activity was observed in the gastrocnemius muscle to counteract forward movement of the center of mass with arm movement. These findings have been replicated for many other postural activities (e.g., Cordo & Nashner, 1982; Marsden, Merton, & Morton, 1978) and they suggest that the nervous system automatically takes into account the consequences of a movement before it occurs. To employ such an anticipatory strategy implies: (1) a continuous monitoring of overall body orientation and; (2) a coherent relationship between body orientation information and anticipatory muscle activity. The development of a prospective form of control in infants implies that they have discovered that sensory information is providing information about their bodies' movements. This may be a significant milestone in motor development as sensory information changes from a natural consequence of a movement to an informational "tool" that the infant may use for
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improving performance. Investigating longitudinally the use of surface support to enhance balance control may reveal this developmental process. The purpose of this study, therefore, is to investigate whether there are developmental changes in how infants use surface contact while standing upright. We begin our longitudinal study when infants are capable of pulling themselves to stand. The acquisition of a new postural orientation (i.e., standing upright) constitutes an opportunity to examine the possible changing relationships between sensory information and overall body control. Specifically, we examine the magnitude of applied contact force, the amount of body sway, and the temporal relationship between applied force and body sway of infants standing upright at four different developmental periods in the acquisition of upright stance. Our hypothesis is that before the acquisition of independent upright stance infants use the contact surface as mechanical support, but with experience in the upright posture, if they are required to maintain contact at a surface, that surface will be used as a source of sensory information to enhance the control of upright stance.
METHOD
Participants Five infants (4 males and 1 female) were the participants in this study and each infant's parent gave written informed consent prior to the infant's participation in the study. Infants were recruited from friends and students at the University of Maryland. All infants were born into middle class families of Euro-American background. These infants were examined monthly, with a few exceptions, from when they were able to stand with support to after independent walking acquisition. Four developmental periods were used to group the data based on each infant's motor milestones: (a) pull to stand (PS), the developmental period in
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TABLE 1 D e v e l o p m e n t a l Periods and Corresponding Ages of Infants in Weeks
Infant
PS
5,4
WO
PW
1
42 (3) 45 (3) 44 (3) 46 (3)
48 (3) --
52 (3) 53 (3) 54 (3) 56 (3)
58 (3) 58 (3) --
52 (1) 53.4
57 (3) 58.5
1.6
1.7
2 3 4
49 (3) --
5
--
M
44.2
49 (2) 48.6
SD
1.7
0.5
61 (3)
Numbers in parentheses indicate the number of usable segments (seetext for criteria) for infants in the specific developmental period. PS = pull to stand, SA = stand alone, WO = walking onset, and PW = post-walking. Dash (--) indicates that data were not obtained for the infant at that developmental period.
which the infant was able to pull to stand by himself or herself with the aid of a supportive surface; (b) stand alone (SA), the developmental period in which the infant was able to stand upright independently for a few seconds without holding or contacting any supportive surface; (c) walking onset (WO), the developmental period in which the infant was able to perform at least three independent walking steps; and (d) post-walking (PW), the developmental period in which the infant was walking independently for approximately 1.5 months of independent walking experience. Information about the milestones was obtained through parent report and verified during the testing visit. Testing was within one week of the milestrone attainment. The infant's age at each developmental milestone is presented in Table 1. Procedures
A brief period of adaptation was allowed when the infant arrived in the laboratory after which he or she was prepared for the experimental session. The infant was placed inside an area surrounded by curtains, forming a "small room" of approximately 1.5 m x 2.5 m. This small room was intended to reduce distraction of the infant's attention by the laboratory envi-
ronment. Inside this room, a rigid hollow wood cube (41 cm wide x 63 cm long x 46 cm high) was clamped to a force platform (Kistler Model 926 IA). This cube had a PVC tube (8 cm diameter) covering one of its sides, providing a cylindrical surface for hand contact. A 1.45 cm high wood platform (45 c m x 61 cm) was placed on the floor beside the cube. Affixed to the platform was a small pedestal (20 cm long x 10 cm deep x 3.5 cm high) on which infants stood. The latter was provided to discourage foot movement. Figure 1 depicts a schematic description of the experimental situation. The infant's task was to stand upright on the pedestal while touching the side of the cube covered by the PVC tube with his or her right hand. We emphasize that even though infants did not require contact with the cube to maintain the upright position after the PS period, they were required to contact the cube in all developmental periods studied. The tube created a round surface that precluded a hand grasp and encouraged a simple placement of the hand and fingers with the palm open. One person was positioned beside the infant preventing possible falls and providing help when necessary. Another person was positioned in front of the infant to help them face forward and stand as quietly as possible. This person showed pictures, books, and toys in an attempt to capture the infant's attention. When the
The Use of 5omatosensory Information
91
-AP !!i]ii~!i! ~!!!,,!ii~
v+ML
'iii;i~gi! :i!! ii::~
+ VER
~iii:i!:!i
i!:~ilill
~
ii:!!!!!!i ii!.!~:ii
,,.~......~ "..,/
Cube
~
Marker on the back !~:ii ,:ii ~
ii:i~iii!il i,;!i igi~i
ili!ii!ii
Force Platform
ii'i~ !i[!!
!~ii i!i!!
ii:iiiiii H~UIU
7
Y
FIGURE 1 Schematic description of an infant standing on the pedestal while contacting the surface. The infant used his or her right hand to contact a cube side covered by a PVC tube. The cube was clamped to a force platform allowing measurement of the applied force in the medial-lateral (ML), anterior-posterior (AP), and vertical (V) directions. The marker on the infant's back was used to estimate the infant's overall body sway.
infant was cooperative, the trial lasted for one minute. The number of trials recorded in each visit varied according to the infant's cooperation. While the infant was standing, the center of mass position and the magnitude of the applied force on the rail of the cube were collected. Due to equipment problems, two procedures were used to collect these data. Fifty-eight percent of the trial segments analyzed in this study were collected by using a video system (Peak Video and Analog Motion Measurement Syst e m - P E A K TM Performance Technologies, Inc.) and 42 percent was collected by using a tracking positional system (3-D Track Posi-
tional System-- Logitech, Inc.). The 3-D tracking positional system consisted of a control unit, a small triangular ultrasonic receiver (7 x 7 x 7 cm), and a triangular transmitter (25 x 25 x 25 cm). The receiver measured body sway in three directions with a resolution of 0.01 cm. When the video system was used, the infant had a reflective marker attached to the back at approximately the center of mass location. Two cameras and two lights were positioned behind and to the side of the infant, making possible the acquisition of the infant's 3D body sway. Neither the cameras nor the lights appeared to interfere with the infants. The force platform data were synchronized with
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
the video image and collected by using the software CODAS (Data Instruments, Inc.). Both video and force data were collected at 60 Hz. After data collection, portions of the trials were selected and the marker placed on the infant's back was digitized to obtain the 3D center of mass information. The criteria for the trial portion selection are discussed later in this section. When the tracking system was used, a receiver was affixed around the infant's waist with a velcro waistband at approximately the center of mass location and an ultrasound transmitter was positioned behind the infant. The tracking system recorded the infant's 3D body sway. Body sway and force data were simultaneously collected by using a custom data acquisition program (LabView) at 50 Hz. The infant's performance was recorded with a video camera positioned in front of him or her to allow the latter identification of quiet stance periods. From both data collection procedures, applied contact force and body sway data were measured and calculated for the side to side or medial-lateral (FMLand CMML),the forward and backward or anterior-posterior (FAp and CMAp), and the up and down or vertical (F v and CMv) directions.
Data Reduction The first step in data reduction was to overlay time series of force and body sway for the same direction (i.e., medial-lateral, anteriorposterior, and vertical). Using the time series and the videotape, the trials were inspected to identify segments for further analysis. Two criteria for identification of such segments were employed.l First, the infant had to stand upright quietly for 10 seconds on the pedestal. During this 10-second period, the infant had to keep both feet on the pedestal and not perform any abrupt movements with his or her arm, trunk, and head. Second, the infant had to maintain contact with the surface with the right hand during the 10-second segment. The goal was to obtain three segments for each session, but this was not always possible because of the
lack of cooperation in standing quietly (see Table 1 for total number of segments per session). If trials included segments longer than 10 s, the first 10 s of the segment was used. For each 10-second segment, mean force and mean sway amplitude of body sway were calculated for medial-lateral, anterior-posterior, and vertical directions. Mean sway amplitude was calculated by subtracting the average of the time series from each data point and obtaining the standard deviation of the time series. In addition to mean force and mean sway amplitude, cross-correlation coefficients between forces and body sway in the same direction (i.e., FML- CMML, FAp-CMAp, and Fv-CMv) were computed. These correlations were performed in both the forward and backward directions to determine the strongest possible coefficients at time lags other than zero. Cross-correlation values were considered valid when maximum coefficients were found with time lags no longer than 450 ms. This maximum time lag value of 450 ms was defined based on previous work on adults showing that the time lag between body sway and applied force in adults is around 300 ms (Jeka & Lackner, 1994, 1995). The time lag window in this experiment is 50% larger than that because infant data may be more variable. If maximum cross-correlation coefficients were found with time lags longer than 450 ms, they were considered missing values in statistical analysis.
Statistical Analysis Valid cross-correlation coefficients were found in all trials (100%) between CMAe-FAp, in 71% of the trials between CMML-FML, and in 66% of the trials between CMv-F v. T-tests revealed that the overall CMAp-FAp and CM vF v coefficients were different from zero (p < .005). This was not the case for CMML-FML coefficients (p > .05). Consequently, only CMAp-FAp and CMv-F v cross-correlation values were considered for further statistical analysis. Four one-way multivariate analyses of variance (MANOVA) were conducted to evaluate differences among the four developmen-
The Use of 5omatosensoty Information
93
15
1~ FML
cde
m
T I0 Z V
c
0
o
e •
d
0 LL
0
PS
SA
WO
PW
Developmental Periods FIGURE2 Mean applied forces collapsed across infants in each developmental period. Applied forces are shown for the three directions: medial-lateral (FML), anterior-posterior if^p), and vertical (Fv). Same letters indicate group means that are significantly different (p< .05). tal periods (PS, SA, WO, and PW). The dependent variables were grouped into four sets: (a) applied force (FML, FAp, and Fv); (b) body sway (CMML, CMAp, and CMv); (c) cross-correlation transformed coefficients2 and time lag values for the anterior-posterior direction (CMAp-FAp); and (d) cross-correlation transformed coefficients and time lag values for the vertical direction (CMv-Fv). Crosscorrelation coefficients and time lags between CMAp-FAp and CMv-F v. were not grouped together because of missing values for the vertical direction. If they have been grouped together, some values for the anterior-posterior direction would have been thrown out. MANOVAs were conducted in each variable group. Since the overall analysis involved four separate MANOVAs, which may inflate Type I error, the level of significance was adjusted by using the Bonferroni procedures for multiple tests. Bonferroni adjustment procedures also were employed in the univariate and post
hoc analyses to keep the overall alpha level at .05.
RESULTS Applied Force Multivariate analysis of variance indicated that there were significant differences in applied force across the four developmental periods, Wilks' Lambda = 0.49, F(9,95) = 3.53,p < .001. Figure 2 depicts the mean applied force (FML, FAp, and Fv) across the four developmental periods. Univariate analyses of variance on mean applied force revealed significant differences only for FML,F(3,41) = 4.89, p < .01, and F v, F(3,41) = 10.09, p < .0001. Post hoc analysis showed that applied force in the medial-lateral direction significantly decreased from the PS to the SA and the WO developmental periods. Post hoc analysis on F v revealed that applied contact
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INFANT BEHAVIOR& DEVELOPMENT Vol. 22, No. 1, 1999
2.0
[ ~ CMML
• CMAp
E o
V
~] CMv
ta 1.5
"10
d
E < 1.0 >,,
(~ f"
0.5
0
0.0
PS
SA
WO
PW
Developmental Periods FIGURE3 Mean sway amplitude collapsed across infants in each developmental period. Sway amplitudes are shown for the three directions: medial-lateral (FML), anterior-posterior (FAp), and vertical (Fv). Same letters indicate group means that are significantly different (p < .05).
force in the vertical direction significantly decreased from the PS to the SA, the WO and the PW developmental periods.
BodySway Multivariate analysis of variance revealed significant differences for body sway across the four developmental periods, Wilks' Lambda = 0.45, F(9,95) = 4.02, p < .001. Figure 3 shows the mean sway amplitude (CMML, CMAp, and CMv) across the four developmental periods. Univariate analyses of variance on the mean amplitude sway indicated significant differences for CMML, F(3,41) = 7.86, p < . 0 0 0 5 , and CMAp, F(3,41) = 8.78, p < .0005. Post hoe analyses for both CMML and CMAp revealed that body sway was significantly smaller at the PW than the PS and the WO developmental periods.
BodySwayand Applied Force Correlations F~a,-CMAe:Body sway and applied forces were always positively correlated for the anterior-posterior direction (CMAp-FAp), indicating that as infants swayed forward, for example, applied force increased in this direction and vice versa. Figure 4 shows an exemplar of FAp and CMAp time series from the PS (Fig. 4a) and PW (Fig. 4b) developmental periods. In the PS developmental period, force and body sway are essentially in-phase (for this example, the time lag is zero), meaning that both FAp and CMAp move forward and backward together in time. By contrast, in the PW developmental period, FAp leads CMAp sway by 139 ms. This means that as infants swayed forward, at a certain point the direction of force applied by the hand reversed to a backward direction while body sway continued forward. Approximately 139 ms later, body sway
The Use of SomatosensoryInformation
95
(a) 8
4 Corr = 0.87 Time Lag = 0 ms
4
2
E v
O
zv
0
o. 0
-4
-8
-2
..j
0
2
4
6
O
-4 10
8
Time (sec)
(b) 4
1.0 Corr = 0.79
Time Lag = 139 ms
PAP
1
0.s
2
0.0 n
-0.5 0
-2
-4
, 0
I 2
, •
t 4
,
I 6
,
I 8
,
-1.0 10
Time (sec)
FIGURE4 An exemplar of the time series of CMAp sway (dotted line) and FAp (solid line) in the (a) pulling to stand and (b) post-walking developmental period. Correlation coefficients and time lags for each trial are shown. Note: Different scales are used in (a) and (b) to allow better representation of CMAp and FAp in both developmental periods. Body sway scales are shown on right y-axes of (a) and (b).
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INFANT BEHAVIOR& DEVELOPMENT Vol. 22, No. 1, 1999
0.9
0.3 Q correlation ~ " time lag
¢o
0.8
~
o
o 0.7 O tO ~= 00
I I I
0
0.5 0.4
0.1
PS
SA
WO
"--" v
0.0
i
0.6
k.
0
0.2
t~ t~ ID
E -0.1 iT. -0.2
PW
-0.3
Developmental Periods FIGURE5 Mean cross-correlation coefficients (O) and time lags (*) between applied force and body sway for the anterior-posterior direction (F^p-CM^p) collapsed across infants in each developmental period. Note: Right y-axis corresponds to correlation coefficients and left y-axis corresponds to time lag values.
was reversed to join the contact force in a backward direction. Multivariate analysis of variance of the FApCMAp relationship revealed significant crosscorrelation coefficient and time lag differences across the four developmental periods, Wilks' Lambda = 0.39, F(6,80) = 7.75, p < .001. Figure 5 depicts the cross-correlation coefficients and respective time lag values between FApCMAp across the four developmental periods. Univariate analyses showed that mean correlation coefficients were similar across the four developmental periods but that time lag values were significantly different, F(3,41) = 19.45, p < .0001. Post hoc analysis revealed that time lag values were similar for the first three developmental periods (PS, SA, and WO) but significantly different for the PW developmental period. Whereas in the first three developmental periods applied force was behind body sway by approximately 50 ms, in the PW develop-
mental period applied force was ahead of body sway by approximately 140 ms. Fv-CMv: Multivariate analysis of variance revealed significant cross-correlation coefficient and time lag differences between Fv-CM v across the four developmental periods, Wilks' Lambda = 0.47, F(6,48) = 3.62, p < .006. Figure 6 depicts the cross-correlation coefficients and respective time lag values between F vCM v across the four developmental periods. Univariate analyses showed significant differences only for the cross-correlation coefficients, F(3,25) = 8.87, p < .0005. Post hoc analysis revealed that cross-correlation coefficients were similar for the first three developmental periods (PS, SA, and WO) but significantly different for the PW developmental period. In the first three developmental periods applied force and body sway changes were negatively correlated ( r - -0.6), meaning that as the infants applied more force downward on the
97
The Use of 5omatosensory Information
0.3
0 correlation , ti__melag _
0.5
0.2
e0
0.1 0
0
v
0.0 0.0
t-
°
O ~
Itl -¢)
E -0.1 t--
-0.5 0
0
-0.2
-1.0
PS
SA
WO
PW
-0.3
Developmental Periods FIGURE6 Mean cross-correlation coefficients (O) and time lags (~-) between applied force and body sway for the vertical direction (Fv-CMv) collapsed across infants in each developmental period. Note: Right y-axis corresponds to correlation coefficients and left y-axis corresponds to time lag values. surface they lifted up their body (i.e., the center of mass rose) and vice versa. In the PW developmental period, applied force and body sway were uncorrelated ( r - 0.1, not significantly different from zero, p > .05), meaning that applied force and body sway in the vertical direction were changing independently from each other.
DISCUSSION
Mechanical vs Sensory Support This study examined the functional use of a contact surface by infants during the acquisition of independent bipedal stance. We hypothesized that infants initially use the contact surface for mechanical support and later as a source of sensory information to enhance control of body sway in the upright position. Several aspects of the present results support this hypothesis. First, the magnitude of force
applied on the contact surface in the vertical direction decreased by almost 50% from the PS developmental period to the following developmental periods (SA, WO, and PW), when F v stabilized around 5 N. Although infants are able to produce force with the lower limbs that is sufficient to support their body weight well before the PS developmental period (Roncesvalles & Jensen, 1993), the large applied forces (m 10N) by our infants in the PS developmental period suggests that when they first begin pulling to stand, they require the aid of surrounding objects to maintain a vertical orientation. Only with increased experience in the upright posture (from SA developmental period and later) are they able to reduce their vertical applied forces. It is interesting to note that the decrease in F v on the contact surface, observed from PS to SA, coincides with the period in which infants are acquiring new skills in the upright position. For example, shortly after being able to pull
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
upright by themselves, infants start to cruise (Capute, Shapiro, Palmer, Ross & Wachtel, 1985); a form of moving around, usually laterally, from point to point while holding onto furniture or other support. Clearly, cruising requires: (1) substantial support of the body weight by the lower limbs; (2) that infants shift their weight from one leg to the other as they move from one place to another; and (3) that the hands "give up" the surface as the infant cruises the object. Concomitantly, or shortly after the first cruising experiences, infants also make their first attempts at independent upright stance. Again, independent upright stance demands full support of body weight and control of body segments to keep them aligned in the vertical orientation. Thus, we interpret the decrease in Fv from the PS to SA developmental periods as an indication that infants mastered one of the basic requirements to stand upright, namely, the support and maintenance of body segments over the lower limbs in the vertical orientation (Thelen, Ulrich, & Jensen, 1989). Moreover, once the infants have acquired the ability to support themselves, no dramatic changes in absolute applied force occur in subsequent developmental periods (i.e., WO and PW developmental periods). Second, changes in body sway while the infants were standing upright are also indicative of developmental changes in the use of the contact surface. Despite being able to support the body vertically with less physical support from the contact surface in the SA period, infants still cannot manage the upright position steadily. Body sway magnitude remained the same across the PS, SA, and WO developmental periods, with a significant decrease observed only after walking experience (i.e., in the PW developmental period). For CMML and CMAp,the mean sway amplitude in the PW period decreased over 60% compared to previous developmental periods. Although body sway remained the same across the first three developmental periods (PS, SA, and WO), evidence for improvement in the postural control system can be seen if these findings are taken
together with the decrease observed in applied force. While there was a significant drop in the vertical applied force from PS to SA developmental period, the amount of body sway remained the same. This means that infants were able to maintain equivalent body sway with less applied force at the hand. After some walking experience, postural control further improved as the amount of body sway significantly decreased in the PW developmental period. Postural control improvement in infants over this same period of upright stance development has also been observed by Sveistrup and Woollacott (1996), using a paradigm in which the infant's support surface is perturbed. Their results indicate an improvement in the consistency and organization of automatic postural responses following support surface perturbations as the infants progress from pulling to stand to the attainment of independent walking. Adult-like patterns were well established after a few weeks of independent walking (Sveistrup & Woollacott, 1996). Along with the present results, it is clear that postural control improvements take place during the acquisition of independent upright standing. Over this time, infants are more stable in upright stance with less need for external aid and demonstrate more organized automatic postural responses when their posture is disrupted. We ask then, what is changing during this developmental period as the infant acquires a stable and more organized upright orientation? We suggest these postural control improvements, evidenced by ours and other's results (e.g., Sveistrup & Woollacott, 1996), are associated with development of a coherent relationship between sensory information and motor activity. This means that infants understand the lawful relationship between temporal patterns of sensory information and the control of the body. Consequently, they are now able to use sensory information to improve postural control. Support for this suggestion comes from our third piece of evidence; the analysis of the temporal relationship between applied
The Use of Somatosensory Information
force and body sway. Although cross-correlation coefficients did not reveal any change in the spatial relationship between FAp-CMAp (r --0.65) across developmental periods, crosscorrelation time lags showed a significant change in the temporal relationship between FAp-CMAp. Whereas applied force and body sway were moving nearly in phase during the PS, SA, and WO developmental periods, applied force led body sway by 140 ms during the PW developmental period (Figure 5). This relationship between FAp-CM~a, resembles the relationship between applied force and body sway observed in adults when using fingertip sensory cues to attenuate body sway (Jeka & Lackner, 1994, 1995). This change in time lag suggests that infants are no longer using the contact surface for mechanical support, but are now using somatosensory cues from the hand and fingers contacting the surface to enhance control of body sway. In essence, the applied force signal serves as a model of body sway and, consequently, is used "informationally" to reverse the body's sway. Thus, the temporal relationship between FAp-CMAp illustrates that infants were initially using the contact surface as mechanical support, but later they used it as a source of sensory information. Another indication that infants used the contact surface differently across the developmental periods comes from the relationship between Fv-CM v. Applied force and body sway in the vertical direction were negatively correlated during the PS, SA, and WO developmental periods with time lag values around zero. This relationship indicates, for example, that as infants applied force downward, their body moved upward. This inverse relationship between Fv-CM v resembles a mechanically supportive relationship between the body and the contact surface in which downward forces act as upwardly supportive forces. However, vertically applied force and body sway were uncorrelated in the PW developmental period, indicating that this mechanical relationship is no longer present. Thus, changes in the relationship between both Fv-CM v and FAp-CMAp are observed during the PW developmental
99
period and these changes indicate that the use of contact surface by infants shifted from mechanical support to sensory information.
The Development of Postural Control The present results raise several issues related to the development of postural control. First, what is the nature of the relationship between sensory information and the control of upright stance? And what is the implication of this relationship? Our results revealed that sensory cues from the hand and fingers contacting the surface were used in a feedforward or prospective fashion, meaning that commands to control postural sway are given before sway activity occurs. Although a feedforward scheme has the advantage of far greater stability than a feedback based relationship (Houk & Lehman, 1987), the success of such a feedforward strategy, in postural control, is dependent upon the accuracy of an estimated body orientation model which is used to estimate and anticipate forces acting on the body. For example, center of mass has been suggested as a potential variable which is estimated and used to control postural orientation and equilibrium in adults (Horak & Macpherson, 1996). As infants acquire upright posture, it might be argued that they have developed the ability to estimate and control this variable, implying that they have developed an abstract frame of reference for body orientation. Moreover, when the infants used the contact surface as sensory information, they were able to discriminate applied force changes at the hand and fingers and associate these changes to changes of the center of mass. Because of the fine resolution of the hand and fingers for precise estimation of force changes, force signals at the hand and fingers provided information about body sway even when it is minimal, allowing for anticipatory postural corrections. Thus, the development of this feedforward relationship between body sway and sensory information based upon an internal frame of reference for body orientation seems to be a crucial piece for the development of postural control.
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
A second issue raised by our results is the question of why infants change their use of the contact surface? Initially infants use the contact surface for mechanical support, but by the time they were experienced independent walkers, their results were similar to those from adults lightly touching a contact surface (Jeka & Lackner, 1994, 1995). Of course the adults were instructed to use light touch (i.e., apply < 1 N of force on the contact surface), whereas the infants spontaneously decreased applied force levels on the Contact surface. Perhaps they naturally adopt their own version of "light touch ''3 to contact the surface, in response to their motivation to stand upright independently without mechanical support from surrounding objects. This motivation could be related to the increased functional activity it affords. For example, leaning on a surface may restrict the immediate mobility in such a way that the body needs to be re-oriented before moving to an object or location of interest (e.g., a toy). With light touch, there is no such need. Movement to an object of interest can begin immediately with the freedom to move in any direction. Thus, giving up mechanical support from surrounding objects as a consequence of postural control improvements may provide the infant with more functional mobility in the environment. Finally, why did the use of the contact surface as a source of sensory information emerge approximately one to two months after walking onset? One possible explanation is that at walking onset, infants have not developed the frame of reference that would allow for the control of the center of mass in the upright position. That is, even though they can stand independently and take three unassisted walking steps (our marker of walking onset), the infants need experience with a wider range of dynamic postural adjustments that several months of walking practice affords. In fact, the onset of walking is characterized by limited mobility as well as intralimb and interlimb patterns that are limited by postural demands (Clark & Phillips, 1993; Clark, Whitall & Phillips, 1988). Walking independently frees the arms from relying
on contact surfaces for support, sensory or mechanical. However as our paradigm reveals, postural control with hand contact allows one to observe the feedforward or prospective temporal relationship that has developed concurrently with a more stable walking pattern. In this view, postural control and walking reinforce each other during the first years of life. Indeed, posture may not be a rate limiter to walking as has been suggested (Thelen, 1986), but rather a co-developing system. In sum, we have showed that infants use a contact surface differently as they acquire the upright stance. After some experience of independent walking, the contact surface can be used as a source of information for body orientation. We suggest that the development of a feedforward relationship between sensory information and motor action is one of the processes underlying developmental changes in postural control. This requires that infants are able to estimate and control the center of mass, a calculated variable that implies the development of an internal representation of body orientation. Acknowledgments: J.A. Barela was sponsored by Conselho Nacional de Desenvolvimento Cientifico--CNPq. Doctoral Program Grant--Brazilian Government. Process # 200952/93.5. Portions of this research have been presented at the 26 th Annual Meeting of the Society for Neuroscience, the annual conference of the North American Society for the Psychology of Sport and Physical Activity, Denver, 1997; and the 13th International Symposium on Posture and Gait, Pads, 1997. The authors wish to express their gratitude to the infants and their parents who gave willing of their time and effort. A special acknowledgment to Z. J. who taught us much about how to design this experiment.
NOTES 1. These two criteria were also used to define the trial portions digitized when the video system was used.
The Use of SomatosensoryInformation
2. The cross-correlation coefficients were first
3.
transformed to the Fisher's z scores. This transformation is necessary because cross-correlations coefficients do not have a normal distribution. According to Winter (1990), an adult's arm weights about 5% of the total body weight. Applying this proportionality, the arm weight of infants in this experiment can be roughly estimated as 0.5 Kg (total body weight - 1 0 Kg) that if placed passively on a surface would produce a force of 5 N on the vertical direction (0.5 Kg ~, 5.1 N). Thus, even at the observed force levels of 5 N, it is still reasonable to assume that infants are just placing their arm on the surface using "light touch."
REFERENCES
Ashmead, D. H., & McCarty, M. E. (1991). Postural sway of human infants while standing in light and dark. Child Development, 62, 1276--1287. Belenkii, Y. Y., Gurfinkel, V., & Paltsev, Y. I. (1967). Element of control of voluntary movements. Biofizika, 12, 135-141. Bertenthal, B. I., & Clifton, R. K. (1998). Perception and action. In D. Kuhn & R. Siegler (Eds.),
Handbook of Child Psychology. Vol. 2. Cognition, Perception and Language (pp. 51-102). New York: Wiley. Capute, A. J., Shapiro, B. K., Palmer, F. B., Ross, A., & Wachtel, R. C. (1985). Normal gross motor development: The influences of race, sex and socio-economic status. Developmental Medicine and Child Neurology, 39, 635-643. Clark, J. E., & Phillips, S. J. (1993). A longitudinal study of intralimb coordination in the first year of independent walking: A dynamical systems analysis. Child Development, 64, 1143- 1157. Clark, J. E., Whitall, J., & Phillips, S. J. (1988). Human interlimb coordination: The first 6 months of independent walking. Developmental Psychobiology, 21, 445--456. Cordo, P. J., & Nashner, L. M. (1982). Properties of postural movements related to a voluntary movement. Journal of Neurophysiology, 47, 287-303. Frankenburg, W. K., Dodds, J., Archer, P., Shapiro, H., & Bresnick, B. (1992). The Denver II: A major revision and restandardization of the Denver Developmental Screening Test. Pediatrics, 89, 91-97.
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Holden, M., Ventura, J., & Lackner, J. R. (1994). Stabilization of posture by precision contact of the index finger. Journal of Vestibular Research, 4, 285-301. Horak, F. B., & Macpherson, J. M. (1996). Postural orientation and equilibrium. In L. B. Rowell & J. T. Shepherd (Eds.), Handbook of physiology (pp. 255-292). New York: Oxford University Press. Houk, J. C., & Lehman, S. (1987). Control systems: Feedback, feedforward, and adaptive strategies. In G. Adelman (Ed.), Encyclopedia of neuroscience (pp. 275-277). Boston, MA: Birk Kauser. Jeka, J. J., & Lackner, J. R. (1994). Fingertip contact influences human postural control. Experimental Brain Research, 100, 495-502. Jeka, J. J., & Lackner, J. R. (1995). The role of haptic cues from rough and slippery surfaces in human postural control. Experimental Brain Research, 103, 267-276. Marsden, C. D., Merton, P. A., & Morton, H. B. (1978). Anticipatory postural responses in the human subject. Journal of Physiology, 275, 47P--48P. Nashner, L. M. (1981). Analysis of stance posture in humans. In A. L. Towe & E. S. Luschei (Eds.),
Motor coordination. Handbook of behavioral neurology (Vol. 5, pp. 527-565). New York: Plenum Press. Roncesvalles, N. C., & Jensen, J. L. (1993). The expression of weight-beating ability in infants between four and seven months of age. Journal of Sport and Exercise Psychology, 15, $68. Sveistrup, H., & Woollacott, M. H. (1996). Longitudinal development of the automatic postural responses in infants. Journal of Motor Behavior, 28, 58-70. Thelen, E. (1986). Development of coordinated movement: Implications for early human development. In M. G. Wade & H. T. A. Whiting (Eds.), Motor development in children: Aspects of coordination and control (pp. 106-119). Boston, MA: Martin Nijhoff. Thelen, E., Ulrich, B. D., & Jensen, J. L. (1989). The developmental origins of locomotion. In M. H. Woollacott & A. Shumway-Cook (Eds.),
Development of posture and gait: Across the life span (pp. 26--47). Columbia, SC: University of South Carolina Press. von Hofsten, C. (1983). Catching skills in infancy.
Journal of Experimental Psychology: Human Perception and Performance, 9, 75-85.
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von Hofsten, C., & Rosander, K. (1996). The development of gaze control and predictive tracking in young infants. Vision Research, 36, 81-96. von Hofsten, C., & Rosander, K. (1997). Development of smooth pursuit in young infants. Vision Research, 37, 1799-1810. Woollacott, M., Debfi, B., & Mowatt, M. (1987). Neuromuscular control of posture in the infant and child: Is vision dominant? Journal of Motor Behavior, 19, 167-186.
Winter, D. A. (1990). Biomechanics and motor control of human movement. New York: John Wiley & Sons, Inc.
30 December 1997; Revised 18 March 1998 •
John I. leka Jane E. Clark University of Maryland
This study investigated developmental changes in the use of a contact surface during the acquisition of upright posture. Standing infants were longitudinally examined at four developmental epochs: pulling to stand (PS); standing alone (SA); walking onset (WO); and 1.5 months post-walking (PW). The results revealed that as standing experience increased the force applied to the contact surface by the hand and the body sway decreased. Applied force and body sway were consistently related in the anterior-posterior direction (r ~, 0.65). Temporally, body sway led applied force ( - 45ms) at the PS, SA, and WO developmental periods. However, at PW, the temporal relationship reversed and applied force led body sway (~ 140 ms). These results indicate that initially infants use surface contact for mechanical purposes but later for orientation information that affords prospective control of posture.
posture development somatosensory prospective infancy
The acquisition of independent upright stance constitutes a major challenge for young infants to solve. Indeed it is not until around the age of 8 months that infants pull themselves to a stand and near 11 months when they stand independently (Capute, Shapiro, Palmer, Ross, & Wachtel, 1985; Frankenburg, Dodds, Archer,
Shapiro, & Bresnick, 1992). As infants struggle to find a solution to the puzzle of how to stand, they discover that their surrounding environment provides support for their newly emerging posture. For example, before they stand upright independently, infants are often observed using a couch or table for assistance.
• Jane E. Clark, University of Maryland, Department of Kinesiology, College Park, MD, 20741-2611; e-mail: [email protected]. INFANT BEHAVIOR & DEVELOPMENT22 (1), 1999, pp. 87-102 Copyright © 1999 Elsevier Science Inc.
ISSN 0163-6383 All rights of reproduction in any form reserved.
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
In the present paper, we investigate this use of surface contact as infants progress in their ability to stand independently. Our hypothesis is that surface contact initially provides mechanical support, but then becomes a source of sensory information for upright stance orientation that affords anticipatory or prospective control of posture. The postural control system receives information about the body and its environment from three sensory systems: visual, vestibular and somatosensory (Nashner, 1981). Of the three sensory inputs, the visual system has received the most attention in the development of infant postural control (see Bertenthal & Clifton, 1998, for a review). The few developmental studies investigating the role of the vestibular and somatosensory systems have shown well-organized postural responses in the absence of vision. For example, Woollacott, Debfi, and Mowatt (1987) demonstrated that 4-month-olds and older infants with their eyes covered with opaque goggles consistently and correctly activated the appropriate muscles in response to platform perturbations. Moreover, 12- to 14-month-olds are capable of maintaining upright stance in the dark (Ashmead & McCarty, 1991). In both studies, infants performed better when vision was absent, suggesting an important role for somatosensory and vestibular inputs in infants' postural development. The small number of studies on the role of somatosensory and vestibular inputs in infant postural control represents a gap in the infant sensorimotor literature that deserves attention. Part of the reason for this gap may be the difficulty in devising experimental situations that enable postural development in infants to be analyzed. Typically postural tasks require standing quietly for 20-30 seconds. Obviously this is an impossible task for the infant struggling to learn upright postural control. Once quiet standing is achieved, the developmental process may have passed. However recent work by Jeka and Lackner (Holden, Ventura, & Lackner, 1994; Jeka & Lackner, 1994, 1995) suggests an experimental paradigm that
may offer a window into the role of somatosensory information for infant postural development. In these experiments, body sway was significantly attenuated when subjects touched a stationary surface with the right index fingertip. Over 60% of body sway attenuation occurred not only when the fingertip provided mechanical support (5-8 N), but also when force levels were too small (< 1 N) to provide mechanical support of body sway (Holden, Ventura, & Lackner, 1994; Jeka & Lackner, 1994). In both situations, body sway and applied force were spatially correlated, meaning that as the subject swayed toward the contact surface, the applied force increased in that direction and vice versa. However, the temporal relationship between body sway and applied force differed depending on the level of applied force. In the condition in which subjects were allowed to apply as much force as desired (high force), changes in applied force led body sway by less than 100 ms. In the light touch condition (< 1 N of applied force), changes in applied force led body sway by 200-300 ms (Jeka & Lackner, 1994). Further investigation showed appropriate anticipatory postural muscle activity within the 200-300 ms period between changes in force application and body sway (Jeka & Lackner, 1995). Jeka and Lackner (1995) concluded that subjects were extremely sensitive to small force changes at the fingertip and that these changes provide sensory cues used to attenuate body sway through appropriate postural muscle activation. In essence, force changes at the fingertip provide a model of body sway that adults use to activate postural muscles in an anticipatory or feedforward fashion, resulting in attenuated sway. These adult findings offer several implications for postural development in infants. First, the intuitive notion is that infants are deriving mechanical support for the body from contact with a rigid surface (e.g., a coffee table). But this may be true only at the earliest stages of upright support. Another form of 'support' may be the somatosensory information obtained from fingertip and hand contact. Sec-
The Use of Somatosensory Information
ond, the temporal relationship between body sway and contact forces at the hand may signal the onset of prospective control of posture with infants. If infants change their use of the surface contact from mechanical to informational support, then we should expect a similar change in the temporal relationship between applied force and body sway as observed in Jeka and Lackner (1994). Although prospective control has been demonstrated in infants' reaching tasks (von Hofsten, 1983) and in visual pursuit (e.g., von Hofsten & Rosander, 1996, 1997), there is no evidence that prospective or feedforward control is achieved in infants standing upright before they can walk, when walking emerges or after a few months of walking experience. Clearly, feedforward or anticipatory muscle activity provides an important strategy for the postural control system (Houk & Lehman, 1987). Belenkii, Gurfinkel, and Paltsev (1967) illustrated this concept with a simple task of raising the right arm from the hip to a horizontal position at shoulder height while standing. Recordings of EMG activity showed that prior to activity in the right shoulder and arm, a burst of EMG activity was observed in the gastrocnemius muscle to counteract forward movement of the center of mass with arm movement. These findings have been replicated for many other postural activities (e.g., Cordo & Nashner, 1982; Marsden, Merton, & Morton, 1978) and they suggest that the nervous system automatically takes into account the consequences of a movement before it occurs. To employ such an anticipatory strategy implies: (1) a continuous monitoring of overall body orientation and; (2) a coherent relationship between body orientation information and anticipatory muscle activity. The development of a prospective form of control in infants implies that they have discovered that sensory information is providing information about their bodies' movements. This may be a significant milestone in motor development as sensory information changes from a natural consequence of a movement to an informational "tool" that the infant may use for
89
improving performance. Investigating longitudinally the use of surface support to enhance balance control may reveal this developmental process. The purpose of this study, therefore, is to investigate whether there are developmental changes in how infants use surface contact while standing upright. We begin our longitudinal study when infants are capable of pulling themselves to stand. The acquisition of a new postural orientation (i.e., standing upright) constitutes an opportunity to examine the possible changing relationships between sensory information and overall body control. Specifically, we examine the magnitude of applied contact force, the amount of body sway, and the temporal relationship between applied force and body sway of infants standing upright at four different developmental periods in the acquisition of upright stance. Our hypothesis is that before the acquisition of independent upright stance infants use the contact surface as mechanical support, but with experience in the upright posture, if they are required to maintain contact at a surface, that surface will be used as a source of sensory information to enhance the control of upright stance.
METHOD
Participants Five infants (4 males and 1 female) were the participants in this study and each infant's parent gave written informed consent prior to the infant's participation in the study. Infants were recruited from friends and students at the University of Maryland. All infants were born into middle class families of Euro-American background. These infants were examined monthly, with a few exceptions, from when they were able to stand with support to after independent walking acquisition. Four developmental periods were used to group the data based on each infant's motor milestones: (a) pull to stand (PS), the developmental period in
INFANT BEHAVIOR & DEVELOPMENT
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Vol. 22, No. 1, 1999
TABLE 1 D e v e l o p m e n t a l Periods and Corresponding Ages of Infants in Weeks
Infant
PS
5,4
WO
PW
1
42 (3) 45 (3) 44 (3) 46 (3)
48 (3) --
52 (3) 53 (3) 54 (3) 56 (3)
58 (3) 58 (3) --
52 (1) 53.4
57 (3) 58.5
1.6
1.7
2 3 4
49 (3) --
5
--
M
44.2
49 (2) 48.6
SD
1.7
0.5
61 (3)
Numbers in parentheses indicate the number of usable segments (seetext for criteria) for infants in the specific developmental period. PS = pull to stand, SA = stand alone, WO = walking onset, and PW = post-walking. Dash (--) indicates that data were not obtained for the infant at that developmental period.
which the infant was able to pull to stand by himself or herself with the aid of a supportive surface; (b) stand alone (SA), the developmental period in which the infant was able to stand upright independently for a few seconds without holding or contacting any supportive surface; (c) walking onset (WO), the developmental period in which the infant was able to perform at least three independent walking steps; and (d) post-walking (PW), the developmental period in which the infant was walking independently for approximately 1.5 months of independent walking experience. Information about the milestones was obtained through parent report and verified during the testing visit. Testing was within one week of the milestrone attainment. The infant's age at each developmental milestone is presented in Table 1. Procedures
A brief period of adaptation was allowed when the infant arrived in the laboratory after which he or she was prepared for the experimental session. The infant was placed inside an area surrounded by curtains, forming a "small room" of approximately 1.5 m x 2.5 m. This small room was intended to reduce distraction of the infant's attention by the laboratory envi-
ronment. Inside this room, a rigid hollow wood cube (41 cm wide x 63 cm long x 46 cm high) was clamped to a force platform (Kistler Model 926 IA). This cube had a PVC tube (8 cm diameter) covering one of its sides, providing a cylindrical surface for hand contact. A 1.45 cm high wood platform (45 c m x 61 cm) was placed on the floor beside the cube. Affixed to the platform was a small pedestal (20 cm long x 10 cm deep x 3.5 cm high) on which infants stood. The latter was provided to discourage foot movement. Figure 1 depicts a schematic description of the experimental situation. The infant's task was to stand upright on the pedestal while touching the side of the cube covered by the PVC tube with his or her right hand. We emphasize that even though infants did not require contact with the cube to maintain the upright position after the PS period, they were required to contact the cube in all developmental periods studied. The tube created a round surface that precluded a hand grasp and encouraged a simple placement of the hand and fingers with the palm open. One person was positioned beside the infant preventing possible falls and providing help when necessary. Another person was positioned in front of the infant to help them face forward and stand as quietly as possible. This person showed pictures, books, and toys in an attempt to capture the infant's attention. When the
The Use of 5omatosensory Information
91
-AP !!i]ii~!i! ~!!!,,!ii~
v+ML
'iii;i~gi! :i!! ii::~
+ VER
~iii:i!:!i
i!:~ilill
~
ii:!!!!!!i ii!.!~:ii
,,.~......~ "..,/
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~
Marker on the back !~:ii ,:ii ~
ii:i~iii!il i,;!i igi~i
ili!ii!ii
Force Platform
ii'i~ !i[!!
!~ii i!i!!
ii:iiiiii H~UIU
7
Y
FIGURE 1 Schematic description of an infant standing on the pedestal while contacting the surface. The infant used his or her right hand to contact a cube side covered by a PVC tube. The cube was clamped to a force platform allowing measurement of the applied force in the medial-lateral (ML), anterior-posterior (AP), and vertical (V) directions. The marker on the infant's back was used to estimate the infant's overall body sway.
infant was cooperative, the trial lasted for one minute. The number of trials recorded in each visit varied according to the infant's cooperation. While the infant was standing, the center of mass position and the magnitude of the applied force on the rail of the cube were collected. Due to equipment problems, two procedures were used to collect these data. Fifty-eight percent of the trial segments analyzed in this study were collected by using a video system (Peak Video and Analog Motion Measurement Syst e m - P E A K TM Performance Technologies, Inc.) and 42 percent was collected by using a tracking positional system (3-D Track Posi-
tional System-- Logitech, Inc.). The 3-D tracking positional system consisted of a control unit, a small triangular ultrasonic receiver (7 x 7 x 7 cm), and a triangular transmitter (25 x 25 x 25 cm). The receiver measured body sway in three directions with a resolution of 0.01 cm. When the video system was used, the infant had a reflective marker attached to the back at approximately the center of mass location. Two cameras and two lights were positioned behind and to the side of the infant, making possible the acquisition of the infant's 3D body sway. Neither the cameras nor the lights appeared to interfere with the infants. The force platform data were synchronized with
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INFANT BEHAVIOR & DEVELOPMENT Vol. 22, No. 1, 1999
the video image and collected by using the software CODAS (Data Instruments, Inc.). Both video and force data were collected at 60 Hz. After data collection, portions of the trials were selected and the marker placed on the infant's back was digitized to obtain the 3D center of mass information. The criteria for the trial portion selection are discussed later in this section. When the tracking system was used, a receiver was affixed around the infant's waist with a velcro waistband at approximately the center of mass location and an ultrasound transmitter was positioned behind the infant. The tracking system recorded the infant's 3D body sway. Body sway and force data were simultaneously collected by using a custom data acquisition program (LabView) at 50 Hz. The infant's performance was recorded with a video camera positioned in front of him or her to allow the latter identification of quiet stance periods. From both data collection procedures, applied contact force and body sway data were measured and calculated for the side to side or medial-lateral (FMLand CMML),the forward and backward or anterior-posterior (FAp and CMAp), and the up and down or vertical (F v and CMv) directions.
Data Reduction The first step in data reduction was to overlay time series of force and body sway for the same direction (i.e., medial-lateral, anteriorposterior, and vertical). Using the time series and the videotape, the trials were inspected to identify segments for further analysis. Two criteria for identification of such segments were employed.l First, the infant had to stand upright quietly for 10 seconds on the pedestal. During this 10-second period, the infant had to keep both feet on the pedestal and not perform any abrupt movements with his or her arm, trunk, and head. Second, the infant had to maintain contact with the surface with the right hand during the 10-second segment. The goal was to obtain three segments for each session, but this was not always possible because of the
lack of cooperation in standing quietly (see Table 1 for total number of segments per session). If trials included segments longer than 10 s, the first 10 s of the segment was used. For each 10-second segment, mean force and mean sway amplitude of body sway were calculated for medial-lateral, anterior-posterior, and vertical directions. Mean sway amplitude was calculated by subtracting the average of the time series from each data point and obtaining the standard deviation of the time series. In addition to mean force and mean sway amplitude, cross-correlation coefficients between forces and body sway in the same direction (i.e., FML- CMML, FAp-CMAp, and Fv-CMv) were computed. These correlations were performed in both the forward and backward directions to determine the strongest possible coefficients at time lags other than zero. Cross-correlation values were considered valid when maximum coefficients were found with time lags no longer than 450 ms. This maximum time lag value of 450 ms was defined based on previous work on adults showing that the time lag between body sway and applied force in adults is around 300 ms (Jeka & Lackner, 1994, 1995). The time lag window in this experiment is 50% larger than that because infant data may be more variable. If maximum cross-correlation coefficients were found with time lags longer than 450 ms, they were considered missing values in statistical analysis.
Statistical Analysis Valid cross-correlation coefficients were found in all trials (100%) between CMAe-FAp, in 71% of the trials between CMML-FML, and in 66% of the trials between CMv-F v. T-tests revealed that the overall CMAp-FAp and CM vF v coefficients were different from zero (p < .005). This was not the case for CMML-FML coefficients (p > .05). Consequently, only CMAp-FAp and CMv-F v cross-correlation values were considered for further statistical analysis. Four one-way multivariate analyses of variance (MANOVA) were conducted to evaluate differences among the four developmen-
The Use of 5omatosensoty Information
93
15
1~ FML
cde
m
T I0 Z V
c
0
o
e •
d
0 LL
0
PS
SA
WO
PW
Developmental Periods FIGURE2 Mean applied forces collapsed across infants in each developmental period. Applied forces are shown for the three directions: medial-lateral (FML), anterior-posterior if^p), and vertical (Fv). Same letters indicate group means that are significantly different (p< .05). tal periods (PS, SA, WO, and PW). The dependent variables were grouped into four sets: (a) applied force (FML, FAp, and Fv); (b) body sway (CMML, CMAp, and CMv); (c) cross-correlation transformed coefficients2 and time lag values for the anterior-posterior direction (CMAp-FAp); and (d) cross-correlation transformed coefficients and time lag values for the vertical direction (CMv-Fv). Crosscorrelation coefficients and time lags between CMAp-FAp and CMv-F v. were not grouped together because of missing values for the vertical direction. If they have been grouped together, some values for the anterior-posterior direction would have been thrown out. MANOVAs were conducted in each variable group. Since the overall analysis involved four separate MANOVAs, which may inflate Type I error, the level of significance was adjusted by using the Bonferroni procedures for multiple tests. Bonferroni adjustment procedures also were employed in the univariate and post
hoc analyses to keep the overall alpha level at .05.
RESULTS Applied Force Multivariate analysis of variance indicated that there were significant differences in applied force across the four developmental periods, Wilks' Lambda = 0.49, F(9,95) = 3.53,p < .001. Figure 2 depicts the mean applied force (FML, FAp, and Fv) across the four developmental periods. Univariate analyses of variance on mean applied force revealed significant differences only for FML,F(3,41) = 4.89, p < .01, and F v, F(3,41) = 10.09, p < .0001. Post hoc analysis showed that applied force in the medial-lateral direction significantly decreased from the PS to the SA and the WO developmental periods. Post hoc analysis on F v revealed that applied contact
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INFANT BEHAVIOR& DEVELOPMENT Vol. 22, No. 1, 1999
2.0
[ ~ CMML
• CMAp
E o
V
~] CMv
ta 1.5
"10
d
E < 1.0 >,,
(~ f"
0.5
0
0.0
PS
SA
WO
PW
Developmental Periods FIGURE3 Mean sway amplitude collapsed across infants in each developmental period. Sway amplitudes are shown for the three directions: medial-lateral (FML), anterior-posterior (FAp), and vertical (Fv). Same letters indicate group means that are significantly different (p < .05).
force in the vertical direction significantly decreased from the PS to the SA, the WO and the PW developmental periods.
BodySway Multivariate analysis of variance revealed significant differences for body sway across the four developmental periods, Wilks' Lambda = 0.45, F(9,95) = 4.02, p < .001. Figure 3 shows the mean sway amplitude (CMML, CMAp, and CMv) across the four developmental periods. Univariate analyses of variance on the mean amplitude sway indicated significant differences for CMML, F(3,41) = 7.86, p < . 0 0 0 5 , and CMAp, F(3,41) = 8.78, p < .0005. Post hoe analyses for both CMML and CMAp revealed that body sway was significantly smaller at the PW than the PS and the WO developmental periods.
BodySwayand Applied Force Correlations F~a,-CMAe:Body sway and applied forces were always positively correlated for the anterior-posterior direction (CMAp-FAp), indicating that as infants swayed forward, for example, applied force increased in this direction and vice versa. Figure 4 shows an exemplar of FAp and CMAp time series from the PS (Fig. 4a) and PW (Fig. 4b) developmental periods. In the PS developmental period, force and body sway are essentially in-phase (for this example, the time lag is zero), meaning that both FAp and CMAp move forward and backward together in time. By contrast, in the PW developmental period, FAp leads CMAp sway by 139 ms. This means that as infants swayed forward, at a certain point the direction of force applied by the hand reversed to a backward direction while body sway continued forward. Approximately 139 ms later, body sway
The Use of SomatosensoryInformation
95
(a) 8
4 Corr = 0.87 Time Lag = 0 ms
4
2
E v
O
zv
0
o. 0
-4
-8
-2
..j
0
2
4
6
O
-4 10
8
Time (sec)
(b) 4
1.0 Corr = 0.79
Time Lag = 139 ms
PAP
1
0.s
2
0.0 n
-0.5 0
-2
-4
, 0
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t 4
,
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-1.0 10
Time (sec)
FIGURE4 An exemplar of the time series of CMAp sway (dotted line) and FAp (solid line) in the (a) pulling to stand and (b) post-walking developmental period. Correlation coefficients and time lags for each trial are shown. Note: Different scales are used in (a) and (b) to allow better representation of CMAp and FAp in both developmental periods. Body sway scales are shown on right y-axes of (a) and (b).
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INFANT BEHAVIOR& DEVELOPMENT Vol. 22, No. 1, 1999
0.9
0.3 Q correlation ~ " time lag
¢o
0.8
~
o
o 0.7 O tO ~= 00
I I I
0
0.5 0.4
0.1
PS
SA
WO
"--" v
0.0
i
0.6
k.
0
0.2
t~ t~ ID
E -0.1 iT. -0.2
PW
-0.3
Developmental Periods FIGURE5 Mean cross-correlation coefficients (O) and time lags (*) between applied force and body sway for the anterior-posterior direction (F^p-CM^p) collapsed across infants in each developmental period. Note: Right y-axis corresponds to correlation coefficients and left y-axis corresponds to time lag values.
was reversed to join the contact force in a backward direction. Multivariate analysis of variance of the FApCMAp relationship revealed significant crosscorrelation coefficient and time lag differences across the four developmental periods, Wilks' Lambda = 0.39, F(6,80) = 7.75, p < .001. Figure 5 depicts the cross-correlation coefficients and respective time lag values between FApCMAp across the four developmental periods. Univariate analyses showed that mean correlation coefficients were similar across the four developmental periods but that time lag values were significantly different, F(3,41) = 19.45, p < .0001. Post hoc analysis revealed that time lag values were similar for the first three developmental periods (PS, SA, and WO) but significantly different for the PW developmental period. Whereas in the first three developmental periods applied force was behind body sway by approximately 50 ms, in the PW develop-
mental period applied force was ahead of body sway by approximately 140 ms. Fv-CMv: Multivariate analysis of variance revealed significant cross-correlation coefficient and time lag differences between Fv-CM v across the four developmental periods, Wilks' Lambda = 0.47, F(6,48) = 3.62, p < .006. Figure 6 depicts the cross-correlation coefficients and respective time lag values between F vCM v across the four developmental periods. Univariate analyses showed significant differences only for the cross-correlation coefficients, F(3,25) = 8.87, p < .0005. Post hoc analysis revealed that cross-correlation coefficients were similar for the first three developmental periods (PS, SA, and WO) but significantly different for the PW developmental period. In the first three developmental periods applied force and body sway changes were negatively correlated ( r - -0.6), meaning that as the infants applied more force downward on the
97
The Use of 5omatosensory Information
0.3
0 correlation , ti__melag _
0.5
0.2
e0
0.1 0
0
v
0.0 0.0
t-
°
O ~
Itl -¢)
E -0.1 t--
-0.5 0
0
-0.2
-1.0
PS
SA
WO
PW
-0.3
Developmental Periods FIGURE6 Mean cross-correlation coefficients (O) and time lags (~-) between applied force and body sway for the vertical direction (Fv-CMv) collapsed across infants in each developmental period. Note: Right y-axis corresponds to correlation coefficients and left y-axis corresponds to time lag values. surface they lifted up their body (i.e., the center of mass rose) and vice versa. In the PW developmental period, applied force and body sway were uncorrelated ( r - 0.1, not significantly different from zero, p > .05), meaning that applied force and body sway in the vertical direction were changing independently from each other.
DISCUSSION
Mechanical vs Sensory Support This study examined the functional use of a contact surface by infants during the acquisition of independent bipedal stance. We hypothesized that infants initially use the contact surface for mechanical support and later as a source of sensory information to enhance control of body sway in the upright position. Several aspects of the present results support this hypothesis. First, the magnitude of force
applied on the contact surface in the vertical direction decreased by almost 50% from the PS developmental period to the following developmental periods (SA, WO, and PW), when F v stabilized around 5 N. Although infants are able to produce force with the lower limbs that is sufficient to support their body weight well before the PS developmental period (Roncesvalles & Jensen, 1993), the large applied forces (m 10N) by our infants in the PS developmental period suggests that when they first begin pulling to stand, they require the aid of surrounding objects to maintain a vertical orientation. Only with increased experience in the upright posture (from SA developmental period and later) are they able to reduce their vertical applied forces. It is interesting to note that the decrease in F v on the contact surface, observed from PS to SA, coincides with the period in which infants are acquiring new skills in the upright position. For example, shortly after being able to pull
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upright by themselves, infants start to cruise (Capute, Shapiro, Palmer, Ross & Wachtel, 1985); a form of moving around, usually laterally, from point to point while holding onto furniture or other support. Clearly, cruising requires: (1) substantial support of the body weight by the lower limbs; (2) that infants shift their weight from one leg to the other as they move from one place to another; and (3) that the hands "give up" the surface as the infant cruises the object. Concomitantly, or shortly after the first cruising experiences, infants also make their first attempts at independent upright stance. Again, independent upright stance demands full support of body weight and control of body segments to keep them aligned in the vertical orientation. Thus, we interpret the decrease in Fv from the PS to SA developmental periods as an indication that infants mastered one of the basic requirements to stand upright, namely, the support and maintenance of body segments over the lower limbs in the vertical orientation (Thelen, Ulrich, & Jensen, 1989). Moreover, once the infants have acquired the ability to support themselves, no dramatic changes in absolute applied force occur in subsequent developmental periods (i.e., WO and PW developmental periods). Second, changes in body sway while the infants were standing upright are also indicative of developmental changes in the use of the contact surface. Despite being able to support the body vertically with less physical support from the contact surface in the SA period, infants still cannot manage the upright position steadily. Body sway magnitude remained the same across the PS, SA, and WO developmental periods, with a significant decrease observed only after walking experience (i.e., in the PW developmental period). For CMML and CMAp,the mean sway amplitude in the PW period decreased over 60% compared to previous developmental periods. Although body sway remained the same across the first three developmental periods (PS, SA, and WO), evidence for improvement in the postural control system can be seen if these findings are taken
together with the decrease observed in applied force. While there was a significant drop in the vertical applied force from PS to SA developmental period, the amount of body sway remained the same. This means that infants were able to maintain equivalent body sway with less applied force at the hand. After some walking experience, postural control further improved as the amount of body sway significantly decreased in the PW developmental period. Postural control improvement in infants over this same period of upright stance development has also been observed by Sveistrup and Woollacott (1996), using a paradigm in which the infant's support surface is perturbed. Their results indicate an improvement in the consistency and organization of automatic postural responses following support surface perturbations as the infants progress from pulling to stand to the attainment of independent walking. Adult-like patterns were well established after a few weeks of independent walking (Sveistrup & Woollacott, 1996). Along with the present results, it is clear that postural control improvements take place during the acquisition of independent upright standing. Over this time, infants are more stable in upright stance with less need for external aid and demonstrate more organized automatic postural responses when their posture is disrupted. We ask then, what is changing during this developmental period as the infant acquires a stable and more organized upright orientation? We suggest these postural control improvements, evidenced by ours and other's results (e.g., Sveistrup & Woollacott, 1996), are associated with development of a coherent relationship between sensory information and motor activity. This means that infants understand the lawful relationship between temporal patterns of sensory information and the control of the body. Consequently, they are now able to use sensory information to improve postural control. Support for this suggestion comes from our third piece of evidence; the analysis of the temporal relationship between applied
The Use of Somatosensory Information
force and body sway. Although cross-correlation coefficients did not reveal any change in the spatial relationship between FAp-CMAp (r --0.65) across developmental periods, crosscorrelation time lags showed a significant change in the temporal relationship between FAp-CMAp. Whereas applied force and body sway were moving nearly in phase during the PS, SA, and WO developmental periods, applied force led body sway by 140 ms during the PW developmental period (Figure 5). This relationship between FAp-CM~a, resembles the relationship between applied force and body sway observed in adults when using fingertip sensory cues to attenuate body sway (Jeka & Lackner, 1994, 1995). This change in time lag suggests that infants are no longer using the contact surface for mechanical support, but are now using somatosensory cues from the hand and fingers contacting the surface to enhance control of body sway. In essence, the applied force signal serves as a model of body sway and, consequently, is used "informationally" to reverse the body's sway. Thus, the temporal relationship between FAp-CMAp illustrates that infants were initially using the contact surface as mechanical support, but later they used it as a source of sensory information. Another indication that infants used the contact surface differently across the developmental periods comes from the relationship between Fv-CM v. Applied force and body sway in the vertical direction were negatively correlated during the PS, SA, and WO developmental periods with time lag values around zero. This relationship indicates, for example, that as infants applied force downward, their body moved upward. This inverse relationship between Fv-CM v resembles a mechanically supportive relationship between the body and the contact surface in which downward forces act as upwardly supportive forces. However, vertically applied force and body sway were uncorrelated in the PW developmental period, indicating that this mechanical relationship is no longer present. Thus, changes in the relationship between both Fv-CM v and FAp-CMAp are observed during the PW developmental
99
period and these changes indicate that the use of contact surface by infants shifted from mechanical support to sensory information.
The Development of Postural Control The present results raise several issues related to the development of postural control. First, what is the nature of the relationship between sensory information and the control of upright stance? And what is the implication of this relationship? Our results revealed that sensory cues from the hand and fingers contacting the surface were used in a feedforward or prospective fashion, meaning that commands to control postural sway are given before sway activity occurs. Although a feedforward scheme has the advantage of far greater stability than a feedback based relationship (Houk & Lehman, 1987), the success of such a feedforward strategy, in postural control, is dependent upon the accuracy of an estimated body orientation model which is used to estimate and anticipate forces acting on the body. For example, center of mass has been suggested as a potential variable which is estimated and used to control postural orientation and equilibrium in adults (Horak & Macpherson, 1996). As infants acquire upright posture, it might be argued that they have developed the ability to estimate and control this variable, implying that they have developed an abstract frame of reference for body orientation. Moreover, when the infants used the contact surface as sensory information, they were able to discriminate applied force changes at the hand and fingers and associate these changes to changes of the center of mass. Because of the fine resolution of the hand and fingers for precise estimation of force changes, force signals at the hand and fingers provided information about body sway even when it is minimal, allowing for anticipatory postural corrections. Thus, the development of this feedforward relationship between body sway and sensory information based upon an internal frame of reference for body orientation seems to be a crucial piece for the development of postural control.
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A second issue raised by our results is the question of why infants change their use of the contact surface? Initially infants use the contact surface for mechanical support, but by the time they were experienced independent walkers, their results were similar to those from adults lightly touching a contact surface (Jeka & Lackner, 1994, 1995). Of course the adults were instructed to use light touch (i.e., apply < 1 N of force on the contact surface), whereas the infants spontaneously decreased applied force levels on the Contact surface. Perhaps they naturally adopt their own version of "light touch ''3 to contact the surface, in response to their motivation to stand upright independently without mechanical support from surrounding objects. This motivation could be related to the increased functional activity it affords. For example, leaning on a surface may restrict the immediate mobility in such a way that the body needs to be re-oriented before moving to an object or location of interest (e.g., a toy). With light touch, there is no such need. Movement to an object of interest can begin immediately with the freedom to move in any direction. Thus, giving up mechanical support from surrounding objects as a consequence of postural control improvements may provide the infant with more functional mobility in the environment. Finally, why did the use of the contact surface as a source of sensory information emerge approximately one to two months after walking onset? One possible explanation is that at walking onset, infants have not developed the frame of reference that would allow for the control of the center of mass in the upright position. That is, even though they can stand independently and take three unassisted walking steps (our marker of walking onset), the infants need experience with a wider range of dynamic postural adjustments that several months of walking practice affords. In fact, the onset of walking is characterized by limited mobility as well as intralimb and interlimb patterns that are limited by postural demands (Clark & Phillips, 1993; Clark, Whitall & Phillips, 1988). Walking independently frees the arms from relying
on contact surfaces for support, sensory or mechanical. However as our paradigm reveals, postural control with hand contact allows one to observe the feedforward or prospective temporal relationship that has developed concurrently with a more stable walking pattern. In this view, postural control and walking reinforce each other during the first years of life. Indeed, posture may not be a rate limiter to walking as has been suggested (Thelen, 1986), but rather a co-developing system. In sum, we have showed that infants use a contact surface differently as they acquire the upright stance. After some experience of independent walking, the contact surface can be used as a source of information for body orientation. We suggest that the development of a feedforward relationship between sensory information and motor action is one of the processes underlying developmental changes in postural control. This requires that infants are able to estimate and control the center of mass, a calculated variable that implies the development of an internal representation of body orientation. Acknowledgments: J.A. Barela was sponsored by Conselho Nacional de Desenvolvimento Cientifico--CNPq. Doctoral Program Grant--Brazilian Government. Process # 200952/93.5. Portions of this research have been presented at the 26 th Annual Meeting of the Society for Neuroscience, the annual conference of the North American Society for the Psychology of Sport and Physical Activity, Denver, 1997; and the 13th International Symposium on Posture and Gait, Pads, 1997. The authors wish to express their gratitude to the infants and their parents who gave willing of their time and effort. A special acknowledgment to Z. J. who taught us much about how to design this experiment.
NOTES 1. These two criteria were also used to define the trial portions digitized when the video system was used.
The Use of SomatosensoryInformation
2. The cross-correlation coefficients were first
3.
transformed to the Fisher's z scores. This transformation is necessary because cross-correlations coefficients do not have a normal distribution. According to Winter (1990), an adult's arm weights about 5% of the total body weight. Applying this proportionality, the arm weight of infants in this experiment can be roughly estimated as 0.5 Kg (total body weight - 1 0 Kg) that if placed passively on a surface would produce a force of 5 N on the vertical direction (0.5 Kg ~, 5.1 N). Thus, even at the observed force levels of 5 N, it is still reasonable to assume that infants are just placing their arm on the surface using "light touch."
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30 December 1997; Revised 18 March 1998 •