the development of anticipatory postural adjustments...

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INFANCY, 3(4), 495–517 Copyright © 2002, Lawrence Erlbaum Associates, Inc. The Development of Anticipatory Postural Adjustments in Infancy David C. Witherington University of Virginia Claes von Hofsten and Kerstin Rosander Uppsala University Amanda Robinette University of Virginia Marjorie H. Woollacott University of Oregon Bennett I. Bertenthal University of Chicago Efficient voluntary action requires postural adjustments that compensate for potential balance disturbances before they occur. These anticipatory postural adjustments have been widely investigated in adults, but relatively little is known about their develop- ment, especially during infancy. This study examined the early development of antici- patory postural activity in support of pulling action while standing. A total of 34 infants between 10 and 17 months were tested. The task required infants to open a cabinet drawer to retrieve toys while a force resisting the pulling action was applied to the drawer. The experiment included between 9 and 13 pulling trials. The force resisting the pull was doubled after the first 4 initial trials and returned again to its original value after another 4 trials. Electromyographic activity from the gastrocnemius and biceps brachii muscles was recorded. The proportion of pulls involving anticipatory activity in the gastrocnemius muscles progressively increased between 10 and 17 months. In addition, Requests for reprints should be sent to David C. Witherington, Department of Psychology, Logan Hall, University of New Mexico, Albuquerque, NM 87131. E-mail: [email protected]

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Page 1: The Development of Anticipatory Postural Adjustments …dcnlab/Papers/WitheringtonEtAl(2002)Infancy.pdf · pulling arm, prospectively counteracting an expected forward displacement

INFANCY, 3(4), 495–517Copyright © 2002, Lawrence Erlbaum Associates, Inc.

The Development of AnticipatoryPostural Adjustments in Infancy

David C. WitheringtonUniversity of Virginia

Claes von Hofsten and Kerstin RosanderUppsala University

Amanda RobinetteUniversity of Virginia

Marjorie H. WoollacottUniversity of Oregon

Bennett I. BertenthalUniversity of Chicago

Efficient voluntary action requires postural adjustments that compensate for potentialbalance disturbances before they occur. These anticipatory postural adjustments havebeen widely investigated in adults, but relatively little is known about their develop-ment, especially during infancy. This study examined the early development of antici-patory postural activity in support of pulling action while standing. A total of 34 infantsbetween 10 and 17 months were tested. The task required infants to open a cabinetdrawer to retrieve toys while a force resisting the pulling action was applied to thedrawer. The experiment included between 9 and 13 pulling trials. The force resisting thepull was doubled after the first 4 initial trials and returned again to its original value afteranother 4 trials. Electromyographic activity from the gastrocnemius and biceps brachiimuscles was recorded. The proportion of pulls involving anticipatory activity in thegastrocnemius muscles progressively increased between 10 and 17 months. In addition,

Requests for reprints should be sent to David C. Witherington, Department of Psychology, LoganHall, University of New Mexico, Albuquerque, NM 87131. E-mail: [email protected]

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infants with considerable experience in opening drawers learned to recruit greaterstrength of their anticipatory postural adjustments for heavier pulls. Implications for therole of motoric experience in anticipatory postural activity are discussed.

Every action or movement we make is embedded within a framework of posturalsupport (Gahery & Massion, 1981; Reed, 1989). The form of each action dependscritically on its postural context, and nowhere is this more evident than in theperiod of infancy, when both posture and action undergo major developmentalreorganizations (Bertenthal & Clifton, 1998; Rochat & Bullinger, 1994). Forexample, as posture develops to support the emergence of independent sitting, atransition from predominantly bimanual to predominantly unimanual reaching oc-curs (Rochat, 1992). Neonates, when provided with sufficient head support, per-form precocious reaching movements otherwise absent in the first 1 or 2 monthsof life (Amiel-Tison, 1985; von Hofsten, 1982, 1984). In short, postural support isan integral component of action and its development.

To effectively support action, posture must prepare both infant and adult for thedestabilizing consequences of action (von Hofsten, 1993). Forward movement ofthe arm during a reach, for instance, typically prompts a forward displacement inthe body’s center of gravity that, if not offset, will destabilize the body and under-mine the reaching act itself (Bernstein, 1967). Exclusive reliance on reactive orautomatic postural adjustments—those that respond in feedback fashion to actualdisturbances of postural stability—is inadequate for maintaining an effectivereaching motion, in part because the body’s own inertia produces mechanical lagsthat compromise the utility of adjustments made in the context of existing posturalinstability (von Hofsten, 1993). An additional need exists for postural adjustmentsthat anticipate, in prospective or feed-forward fashion, the disequilibrium that ac-tions produce. Anticipatory postural adjustments establish a compensatory frameof support for action prior to the action itself by estimating postural imbalance andcounteracting the imbalance before it has a chance to occur (Aruin & Latash,1995; Bouisset & Zattara, 1981).

Numerous studies have demonstrated that such prospective adjustments inpostural muscles are fundamental to the adult postural repertoire (Aruin &Latash, 1995; Belen’kii, Gurfinkel, & Pal’tsev, 1967; Breniere, Do, & Bouisset,1987; Commissaris & Toussaint, 1997; Cordo & Nashner, 1982; Lee, 1980).Research on anticipatory postural adjustments most typically features standingadults instructed to raise their arms quickly or pull or push on a manipulandum(e.g., Bouisset & Zattara, 1981; Cordo & Nashner, 1982; Friedli, Hallett, &Simon, 1984; Inglin & Woollacott, 1988). Under these conditions, electromyo-graphic (EMG) activity in the muscles of the legs and trunk reliably precedesactivity in the muscle of the arm by 40 to 60 msec. In the case of a standingadult pulling on a manipulandum, for example, EMG activity in the gastrocne-mius (G) muscles of the lower legs precedes activity in the biceps muscle of the

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pulling arm, prospectively counteracting an expected forward displacement inthe body’s center of gravity.

Anticipatory postural adjustments are an integral facet of voluntary action inadults, critical to the efficiency with which we move and act in the world (vonHofsten, 1993). Such anticipatory activity also marks the postural adjustments ofchildren, who, by 4 to 5 years, reliably demonstrate prospective control of stand-ing posture when asked to stand on tiptoes (Haas, Diener, Rapp, & Dichgans,1989), raise an arm (Riach & Hayes, 1990), unload (Hay & Redon, 1999), initiategait (Assaiante, Woollacott, & Amblard, 2000; Ledebt, Bril, & Breniere, 1998),and pull or push on a handle (Woollacott & Shumway-Cook, 1986), although thetemporal difference between postural activity and arm movement activity underthese conditions is frequently greater and more variable than that found in adults.

In infancy, however, the extent to which anticipatory postural adjustmentsaccompany voluntary action is much less clear. By establishing new means ofpostural control in the head, neck, trunk, and whole body, infants progressivelybuild more elaborate and refined balance frameworks (e.g., self-sitting postures,hands-and-knees crawling postures, and independent standing postures) for sup-porting action. Although postural control is vital to skilled action from birth on-ward (Rochat & Bullinger, 1994), the postural frameworks for infant action may,by and large, involve reactive rather than prospective adjustments, or may incor-porate prospective adjustments only after developmental consolidation of a par-ticular balance frame has occurred. Bernstein (1967), for example, argued thatchildren first rely on reactive postural control to maintain balance during walkingand only gradually establish prospective control. Alternatively, anticipatory pos-tural adjustments may emerge coincident with automatic, feedback posturalmechanisms so that some nascent level of anticipatory activity accompanies thedevelopmental acquisition of each new balance framework in infancy.

Relatively little research to date has examined prospective postural control in in-fants. The only work to examine anticipatory postural adjustments under posturalconditions of independent sitting has yielded discrepant results. Anticipatory pos-tural adjustments during reaching movements in sitting infants were reported byvon Hofsten and Woollacott (1990), who found evidence for anticipatory trunk ex-tensor adjustments in 9-month-old infants. In 19 of 30 cases, trunk extensor firingpreceded deltoid activation. Van der Fits, Otten, Klip, van Eykern, and Hadders-Algra (1999), in contrast, reported very little and highly inconsistent prospectiveactivity in neck extensor, trunk extensor, or hamstrings prior to 15 months.1 Van derFits et al. (1999) used a more stringent criterion for defining anticipatory activitythan that used by von Hofsten and Woollacott (1990), which may contribute to thedisparity between the two sets of results. Nonetheless, strikingly different accounts

ANTICIPATORY POSTURAL ADJUSTMENTS 497

1In an earlier report, van der Fits and Hadders-Algra (1998) reported finding no evidence for con-sistent anticipatory postural activity during seated reaching in infants prior to 18 months.

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for the developmental origins of prospective control during independent sittingarise from these two studies. For von Hofsten and Woollacott, anticipatory posturaladjustments are fundamental to balance control as infants acquire independent sit-ting. For van der Fits et al. (1999), anticipatory postural adjustments play no realrole in the postural support structure for seated reaching until well after independ-ent sitting has been established as a stable postural frame for action.

With the developmental transition to independent standing toward the end ofthe infant’s first year, the need for some measure of prospective postural controlheightens considerably, as the consequences of losing balance in an upright stanceare quite severe relative to other postural frames. Thus, anticipatory posturalcontrol mechanisms for upright stance are especially likely to arise in parallel withthe development of independent standing. Studies of anticipatory postural adjust-ments in standing infants have begun to outline the early development of prospec-tive control in upright stance. Forssberg and Nashner (1982), as part of a largerstudy on the development of automatic postural adjustments, reported data from astanding 1.5-year-old who activated postural muscles before arm muscles when ahandle he was holding was pulled away from him. In a study of 15- to 18-month-olds with under 200 days of walking experience, Breniere, Bril, and Fontaine(1989) recorded evidence of backward shifts in center of pressure prior to the ini-tiation of gait for only 3 of the 8 infants sampled. Recently, however, Assaianteet al. (2000) found that infants within the first 4 months of independent walkingdemonstrate anticipatory lateral weight shifts before initiating gait, suggestingthat some form of prospective control in walking is already present at the onset ofindependent walking.

To date, Barela, Jeka, and Clark (1999) provided the most detailed study ofstanding infants by showing how infants, during the acquisition of upright stance,use a supporting contact surface (a handrail) to prospectively control their balance.Barela et al. (1999) studied infants over four developmental epochs: pulling to stand(10 months), standing alone (11 months), walking onset (12 months), and walkingmastery (13.5 months). Each infant’s body sway and the forces applied to the con-tact surface were measured. Barela et al. found that both body sway and the forcesapplied to the contact surface decreased with increasing upright stance experience.Most important, however, infants during the pulling to stand, standing alone, andwalking onset epochs applied forces to the contact surface as a reaction to or as aphysical consequence of their body sway, whereas infants during the walking mas-tery epoch applied forces to the contact surface in anticipation of body sway.

Although the results of Barela et al. (1999) suggest that prospective control ofstance gradually emerges as infants gain experience with independent standingand, in particular, walking, their study marks only the beginning of a moresystematic study of these issues. The aim of this study was to articulate the earlydevelopmental forms that anticipatory postural adjustments assume in the contextof an action that perturbs the standing posture. A pulling task was chosen. When

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individuals apply a force to pull an object in upright free stance, the G muscles mustcounteract that force ahead of time if the body itself is to resist being pulled towardthe object, thereby upsetting balance. Each infant was given the task of opening acabinet drawer to retrieve toys while different weights resisting the pulling actionwere applied to the drawer. We collected a cross-sectional sample of infants from10 to 17 months to tap a period in development during which infants consolidateboth independent standing and walking. Movements of the drawer and EMG ac-tivity from the G and biceps brachii (B) muscles were recorded during the task.

In keeping with the view that prospective postural control emerges alongsidethe development of different postural frameworks in infancy (von Hofsten &Woollacott, 1990), we hypothesized that, as infants are beginning to stand butwithout support, anticipatory postural adjustments would be present in theirpulling behavior. Thus, between 10 and 17 months, anticipatory postural activ-ity should increase both in the consistency and in the temporal specificity withwhich it supports pulling behavior. In particular, we predicted that the timing ofanticipatory postural adjustments at earlier ages would be more diffuse and lessspecific to pull onset than at later ages. We also hypothesized that earlier formsof anticipatory postural activity would predominately involve activation in bothlegs to provide maximum stability and that as infants increased their use ofprospective postural control they would show less need for such bilateral activa-tion. Finally, based on Forssberg et al.’s (1992) study of developmental changein anticipatory control of gripping during lifting, we predicted that only our old-est infants would demonstrate magnitude adjustments in their anticipatory pos-tural activity to compensate for different weight levels of resistance to pullingbehavior.

METHOD

Participants

Thirty-four infants participated in the experiment. Six infants (3 girls, 3 boys) weretested at 10 months (M = 282 days, range = 280–285 days), 6 (3 girls, 3 boys) at11 months (M = 308 days, range = 304–311 days), 6 (3 girls, 3 boys) at 13 months(M = 367 days, range = 358–370 days), 4 (4 boys) at 14 months (M = 392days, range = 390–395 days), 6 (4 boys, 2 girls) at 15 months (M = 422 days,range = 414–428 days), and 6 (3 boys, 3 girls) at 16 to 17 months (M = 475 days,range = 446–491 days). All participants were healthy, full-term infants (≥ 38 weeksgestational age) from middle- to upper-middle-class families and were predomi-nantly European American. Four additional infants were excluded from analysis: One10- and one 11-month-old did not complete the procedure due to lack of interest, andtwo 14-month-olds did not complete the procedure due to fussiness and crying.

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Apparatus

Infants were positioned facing a wooden, open-backed cabinet measuring 31 cmwide, 51 cm tall, and 46 cm deep (illustrated in Figure 1). The upper half of thecabinet housed a sliding, wooden drawer, measuring 24 cm wide, 9 cm tall, and29 cm deep. The drawer’s handle was positioned 45 cm above the base of the cab-inet, at chest level for most infants between 10 and 17 months. Two rubber stop-pers, attached to the front of the cabinet, provided a 1-cm gap between the closeddrawer and the cabinet frame to prevent the drawer from shutting on infants’hands. When fully opened, the drawer projected a maximum of 17 cm from itsclosed position. At the back of the drawer, inside the cabinet, a wire mesh basketinto which weights could be placed to increase the drawer’s resistance to beingopened was attached via a chain and pulley. Also attached to the back of thedrawer was a 2.5 × 2.5 × 2.0 cm DC magnetic tracker (Ascension Ltd.) designedto register angular and linear displacement in three dimensions, relative to a trans-mitter with a 3.05-m radius range of sensitivity.

Preamplified surface electrodes (G. Westling, Dept. of Physiology, Umeå Uni-versity), attached to the infant, recorded EMG activity of postural muscles, specif-ically, the left and right lateral G, and the primary arm muscles, specifically, the

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FIGURE 1 Drawing of cabinet apparatus, with cross-section revealing the weight basketinside the frame.

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left and right B. Each electrode was placed over the muscle belly of the muscle inquestion. Each electrode signal was full-wave rectified and root mean square(RMS) filtered prior to analysis. Both EMG activity and the displacement of thedrawer were sampled at 50 Hz and time locked with one another.

Procedure

Prior to testing, infants were outfitted with a loose smock to expedite electrodeplacement and maintenance. On the back of the smock was sewn a pocket that se-cured a preamplifier unit into which each electrode directly fed. Once outfitted forthe task and familiarized with the experimenters and setting, the infant was movedto an adjacent room and positioned to face the cabinet. The parent sat on a low boxbehind the infant to provide support for the infant and to help maintain the infant’sattention and positioning toward the task of opening the cabinet drawer. Each par-ent was instructed to provide support to the infant only when necessary and tospecifically support the infant with hands around the infant’s hips to allow for freetrunk and leg movement. An experimenter knelt to one side of the cabinet and, byshowing the infant a toy, placing it in the open drawer, and then closing the drawer,engaged the infant in the activity of opening the drawer to retrieve toys placed in-side. Parents were instructed to keep their infants from trying to open the draweruntil the drawer was closed. Each infant was given two or three practice opportu-nities to open the drawer and remove toys from it before testing began.

A second experimenter videotaped the session from behind a curtained partitionand initiated the sampling of EMG activity and the pulse from the DC magnetictracker. A third experimenter, also positioned behind the partition, monitored thequality of the EMG signals on an oscilloscope to ensure a viable reading and collectedall cables and wires leading from the infant to keep them out of the infant’s way.

Once testing began, each infant received a minimum of 9 drawer opening trialsand a maximum of 13, with 68% of the sample receiving 11 trials. Each triallasted 15 sec, and during the trial, infants were given the opportunity to open thedrawer as many times as they chose. Two weight conditions (227 g and 454 g)were employed during a testing session (4 trials at 227 g, 4 at 454 g, and 3 againat 227) to assess how infants adjust their postural activity to different forms of re-sistance to pulling behavior. Six infants demonstrated some reluctance to open thedrawer under the heavier weight condition. Accordingly, for 2 of these infants(both 10-month-olds), only 227-g trials were collected (10 trials for one infant, 11for the other). For the other 4 infants, only three 454-g trials were administered,with more 227-g trials added to the session.

When we initiated the study, we used a weight contrast of 170 g and 340 g, butafter running the first 4 infants (one 11-, one 16-, and two 13-month-olds), wereplaced these weights with the slightly heavier set of 227 g and 454 g to better

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engage older infants in the task. No muscle force differences surfaced as a func-tion of our using 170-g and 340-g weights for the first 4 participants as opposed tothe standard weights. As a result, pulls involving 170-g and 340-g weights wereincluded under the 227-g and 454-g weight conditions, respectively.

Parents were instructed to ensure that their infants were positioned facing thecabinet, with feet approximately parallel to one another, before the start of eachtrial. Both parents and Experimenter 1 monitored infants’ positioning relative tothe cabinet throughout the session. Infants were considered in position relative tothe cabinet so long as their body and feet orientation remained within approxi-mately 30° of a perfect cabinet-facing position, with feet perpendicular to andbody parallel to the cabinet face. Any trial in which the infant did not open thedrawer or was out of position when opening the drawer was redone.

Following each infant’s testing session, we administered a questionnaire to par-ents about their infants’ motor development. Questions were designed to identifythe number of weeks of experience infants had with independent standing and in-dependent walking. We defined independent standing as the infant’s ability tomaintain a standing position without benefit of any external support for a fewseconds, and independent walking as the infant’s ability to walk at least three stepswithout external support, consistent with motor scale designations in the BayleyScales of Infant Development (Bayley, 1969).

Of the 10-month-olds in our sample, only 1 had independent standing experi-ence (2 weeks). Of the 11-month-olds, only 2 had standing experience (16 weeksand 4 weeks). All remaining 10- and 11-month-olds required one or both hands tosupport their standing. At 13 months, all infants had independent standing experi-ence (M = 6.33, range = 2–12 weeks). Of the 14-month-olds, 3 had standingexperience (14, 18, and 18 weeks) compared to 1 who required both hands to sup-port stance. At 15 months, infants had M = 13.17 weeks of independent standingexperience (range = 5–24 weeks), and by 16 to 17 months, all infants had 10 ormore weeks of standing experience.

No 10-month-olds and only two 11-month-olds had independent walkingexperience (6 weeks and 3 weeks) in our sample. Four of the 6 infants at 13 monthshad independent walking experience (3 with 2 weeks, 1 with 4 weeks), as did 3 ofthe 4 infants at 14 months (8, 10, and 16 weeks). Of the 15-month-olds, 4 of 6 hadwalking experience (8, 12, 16, and 20 weeks), compared to 5 of 6 at 16 to17 months (12, 12, 16, 20, and 22 weeks).

Data Reduction

Pull onset. For the purpose of this study, we isolated translation of thedrawer along one axis of movement to target point of onset for drawer opening.Point of onset for drawer displacement (the “pull” onset) was defined as the first

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point in the time series in which the magnetic tracker registered any forwarddisplacement of the drawer. Videotaped recordings of each session were cross-checked to confirm this designation for every infant pull.

EMG baselines. To establish baseline levels of EMG activity for each ofthe four channels sampled (left and right G and B), we relied on graphical dis-plays of each 15-sec time series, created with the Data Analysis and DisplaySoftware Program from DSP Development. Two coders independently reviewedall sessions. For the first and last trials of every weight condition tested, eachcoder designated a 2-sec baseline period for each channel of EMG activity. Todetermine baseline activity, coders were instructed to isolate 2 consecutive sec ofresting activity at low amplitude levels and with as little signal fluctuation as pos-sible. Baseline onsets falling within 1 sec of each other were designated as anagreement among the coders. Interrater agreement on baseline onset was 85%. Athird coder independently reviewed all disagreements to resolve differencesbetween the other two coders.

Mean levels of activation and standard deviations were computed for each G andB baseline period. First and last trial means and standard deviations were themselvesaveraged to produce a generalized mean and standard deviation for each channel ofbaseline EMG activity applicable to all trials for a given weight condition.

EMG bursts. We set a conservative threshold of 3 SD above mean baseline ac-tivity for the identification of EMG bursts in a 2-sec window (1 sec before, 1 sec afterpull onset). For every trial and every channel of EMG activation, burst activity was de-fined as any above-threshold activity lasting at least 60 msec. The first point abovethreshold for each EMG burst constituted the burst’s onset. Offset of a given EMGburst was defined as the first point of a 100-msec period of activation below threshold.

Anticipatory EMG bursts. We defined an EMG burst in G as an anticipatorypostural adjustment when its onset preceded the pull onset and when its offset oc-curred either after the pull onset or within 100 msec of the pull onset. Anticipatorypostural adjustments (APAs) whose onsets occurred more than 500 msec before thepull onset were designated nonfunctional APAs to reflect their lack of temporalspecificity relative to pull onset. APAs initiated between 260 and 500 msec of pullonset were designated global APAs to reflect their relatively diffuse but functionaltemporal relation to pull onset. Finally, APAs beginning within 240 msec of pull on-set were designated specific APAs to reflect their temporally specific relation to pullonset. The distinction between a global and a specific time region was partly madefor pragmatic reasons and partly based on earlier research. Barela et al. (1999) foundthat the anticipatory force applied to a handrail by postwalking infants led bodysway by 140 msec on average and had an SD of 90 msec. Thus, most of theseadjustments led body sway by 230 msec or less (M + SD). Similar figures were

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obtained by von Hofsten and Woollacott (1990) when examining the preparatory ac-tivation of the trunk muscles in infants reaching for an object when in an unstableposture. We thus defined each infant pull in terms of the anticipatory nature of ac-tivity observed in left or right G. Those pulls for which infants did not demonstrateAPAs as defined here were designated no APA. For each infant, proportions forthese pattern designations were computed by dividing the number of pulls charac-terized by a particular pattern by the total number of pulls.

Due to interference in the signal, 21 total pulls (4% of the total sample) wereeliminated prior to analysis: 3 pulls at 10 months, 4 at both 11 and 16 to17 months, 6 at 13 months, and 2 at both 14 and 15 months. On average, 10-month-olds in the sample pulled the drawer open 16.33 times (SD = 3.44)during their sessions. At 11 months, the mean number of pulls was also 16.33(SD = 5.39); at 13 months, 12.83 (SD = 3.43); at 14 months, 14.50 (SD = 5.07);at 15 months, 15.17 (SD = 2.79); and at 16 to 17 months, 14.83 (SD = 1.83).

Preliminary analyses yielded no significant main effects of sex on infant anticipa-tory activity; therefore, in subsequent analyses, we collapsed all data across gender.

RESULTS

Figure 2 provides a single pull illustration of EMG burst activity in left G, right G,and B for an infant at 10 months contrasted with an infant at 16 months. In the fol-lowing analyses, the proportion of pulls characterized by various pattern designa-tions for each infant served as the primary variable of interest for investigating thedevelopmental course of anticipatory postural adjustments under standing condi-tions. All proportions were derived from the total number of pulls available foreach infant, totaled across weight conditions. Proportional data were arcsinetransformed prior to analysis to normalize distributions.

Age Changes in Anticipatory Activity of Postural Muscles

We first looked at age changes in the proportion of pulls for pattern designationsof no APA, nonfunctional APA, global APA, and specific APA irrespective of thepostural muscle (left vs. right G) involved. Figure 3 presents mean proportionsfor each APA pattern across six ages. A trend analysis performed on these pro-portions yielded evidence for a significant linear trend component across age inspecific APA, F(1, 28) = 13.27, p < .005; global APA, F(1, 28) = 8.15, p < .01;and no APA, F(1, 28) = 10.43, p < .005. No other trend components reached sta-tistical significance at an � level of .05, although a cubic trend across age in noAPA approached significance, F(1, 28) = 4.02, p = .055. Inspection of Figure 3reveals a progressive increase in the proportion of infant pulls employing specific

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505

FIGURE 2 Two single-pull samples of electromyographic (EMG) bursts in left gastrocne-mius (LG), right gastrocnemius (RG), and prime mover biceps brachii (B) muscles for (a) aninfant at 10 months and (b) an infant at 16 months. One second of EMG activity for each infantis displayed, 800 msec of which feature activity prior to pull onset (designated as 0) and200 msec of which feature activity at and subsequent to pull onset.

a)

b)

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APA between 10 and 17 months, marked by a period between 13 and 15 monthsof relative stasis in the upward trend. By 16 to 17 months, infants employedspecific APA in over half of their pulls (M = .56, SD = .13) as compared to lessthan one-fourth of their pulls at 10 months (M = .22, SD = .08). A much moregradual upward trend characterized age-related changes in global APA. Pairedsamples t tests at each age comparing the proportion of pulls marked by specificAPA with those marked by global APA yielded significant differences only for16- to 17-month-olds, t(5) = 3.44, p < .05. Thus, prior to 16 months, specific APAdoes not predominate over global APA in infants’ anticipatory activity.

The proportion of infant pulls involving no APA steadily declined between10 and 17 months, reaching a plateau after 14 months. This plateau in trend,coupled with an initial rise in no APA responding between 10 and 11 months,contribute to the suggestion of a possible cubic component to these data acrossage. In particular, infants at 11 months exhibited both the highest mean propor-tion of pulls involving no APA and the largest range of variation in responding

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FIGURE 3 Mean proportion of pulls (+SE) involving general designations of anticipatorypostural activity for each of six age groups.

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(M = .56, SD = .38), suggesting the importance of 11 months as a time of transi-tion in the development of anticipatory postural adjustments.

Combining specific APA and global APA under a general functional APA cate-gory, defined as anticipatory activity initiated within 500 msec of pull onset, of-fers further evidence for a progressive increase in utilization of anticipatory pos-tural adjustments between 10 and 17 months. A trend analysis on functional APAyielded a significant linear component across age, F(1, 28) = 24.84, p < .001.Functional APA characterized about one third of infants’ pulls at 10 (M = .37,SD = .08) and 11 months (M = .33, SD = .27), nearly two thirds of infants’ pullsby 13 (M = .65, SD = .19) and 14 months (M = .61, SD = .27), and around threefourths of infants’ pulls at 15 (M = .74, SD = .18) and 16 to 17 months (M = .82,SD = .10). Beginning at 13 months, the proportion of infants’ pulls involving func-tional APA was significantly higher than the proportion of pulls involving no APA,t(5) = 2.87, p < .05. Thus, by 13 months, when all infants in our sample were gain-ing independent standing experience, the majority of infants’ pulls were markedby some degree of prospective postural control. From 15 months onward, the pro-portion of infants’ pulls marked by specific APA was significantly higher than theproportion of pulls marked by no APA, ts(5) > 4.13, ps < .01.

Coherence in anticipatory postural activity across age. We also exam-ined left and right G activity in tandem to determine age-related changes in thecoordination of anticipatory activity across both halves of the postural set. Unilat-eral APA applied to pulls involving either no anticipatory activity or nonfunctionalAPA in one G and functional APA in the other G. Bilateral APA applied to pullsinvolving functional APA in both left and right G. For 46% of pulls involving uni-lateral APA and 47% of pulls involving bilateral APA, infants used both hands toopen the drawer.

Figure 4 presents the mean proportion of pulls for both coordinated APApatterns across age. A trend analysis performed on these proportions yielded evi-dence for a significant linear trend component across age in unilateral APA,F(1, 28) = 10.69, p < .005, and bilateral APA, F(1, 28) = 23.81, p < .001. Addi-tionally, a significant cubic trend component emerged across age in the proportionof infant pulls demonstrating unilateral APA, F(1, 28) = 13.63, p < .001, andbilateral APA, F(1, 28) = 5.75, p < .05. Inspection of Figure 4 reveals an initialdecline in the proportion of pulls demonstrating unilateral APA between 10 and11 months that was reversed between 11 and 13 months. Subsequently, unilateralAPA reached a peak at 15 months (M = .55, SD = .05), only to drop again by 16 to17 months (M = .39, SD = .12). The proportion of pulls demonstrating bilateralAPA rose steadily between 10 and 13 months, then dropped between 13 and14 months, only to rise again between 15 and 16 to 17 months. Thus, between 13and 15 months, a period of decline in the proportion of pulls involving bilateralAPA was juxtaposed against a period of increase in the proportion of pulls marking

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unilateral APA. By 16 to 17 months, infant pulls utilized both unilateral and bilat-eral G activation in roughly equal measure. Infants at 13 months also showed nodifference in the proportion of pulls characterized by unilateral versus bilateralactivity, but at every other age (10, 11, 14, and 15 months), paired samples t testsrevealed significantly greater unilateral activation relative to bilateral activation,ts > 4.10, ps < .01.

Biceps brachii activity across age. Finally, we focused on possible age-related change in the extent to which B served as prime mover for the initiation ofinfant pulls. For this analysis, we defined prepull B activity as any EMG burst inB whose onset occurred within 500 msec of pull onset and whose offset occurredeither at the point of or after pull onset. This criterion was chosen for pragmaticreasons. When infants used both arms to pull open the drawer, we designated thepull as involving prepull B activity if such activity was evident in either right orleft B.

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FIGURE 4 Mean proportion of pulls (+SE) involving functional anticipatory postural activ-ity in both legs (Bilateral) and in only one leg (Unilateral) for each of six age groups.

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A trend analysis on the mean proportion of pulls involving prepull activityrevealed no statistically significant trend components across age. In general,infants for roughly half of their pulls exhibited prepull B activity, suggesting thatB served as prime mover in these instances (M = .48, SD = .17). For each infant,we also computed a mean duration period between prepull B activation and pullonset for those pulls involving prepull B activation. Each mean duration served toindex the specific temporal relation between B activation and pull onset. Acrossages, infants did not differ significantly in when they initiated prepull B activity.On average, infants initiated B activity within 200 msec of pull onset (M = 172.38,SD = 64.31).

Magnitude of Anticipatory Activity in Postural Muscles

The preceding analyses targeted the nature of anticipatory postural activity fromthe standpoint of temporal relations between postural adjustments and pullingbehavior. In the following analyses, we examined the extent to which infants ofdifferent ages adjust the magnitude of their anticipatory activity to compensatefor different forms of resistance to pulling behavior. For each infant, we inte-grated EMG burst activity in each G time series occurring just before pull onsetas an estimate of the average magnitude of anticipatory muscle force applied.Each muscle force estimate included all EMG burst patterning occupying the200 msec immediately prior to pull onset, which is consistent with the criterionof van der Fits and Hadders-Algra (1998). Thus, to provide a full magnitudeestimation, we included in our analyses EMG bursts not terminating within100 msec of pull onset, as long as their burst onset occurred within 200 msec ofpull onset. Muscle force estimates were sampled from the last three pulls occur-ring in the first weight-class condition (227 g) and from the second, third, andfourth pulls occurring in the second weight-class condition (454 g). The firstpull in the second weight-class condition was excluded because on this trial theweight change is still unknown to the infant and could not possibly be antici-pated. We computed an average muscle force estimate across both left and rightG for the first weight-class condition and for the second weight-class condition.The two 10- to 11-month-olds who received only the 227-g weight trials wereeliminated from the sample.

We examined muscle force differences between weight conditions as a functionof age. A series of paired t tests, comparing area estimates across weight conditionfor each age, yielded only one significant effect of condition: at 15 months,t(5) = –3.09, p < .05. Specifically, infants at 15 months exhibited higher areas intheir anticipatory burst activity for the 454-g weight condition (M = 2.99,SD = 2.40) than for the 227-g condition (M = 1.54, SD = .94). No differencesamong conditions at any other age level approached statistical significance. Unlike

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our results chronicling G anticipatory activity, these findings offer little systematicevidence for age differences between 10 and 17 months in the extent to whichinfants adjust their anticipatory postural activity to meet specific task demandssuch as how much resistance accompanies a pull.

Evidence from our sample, however, suggests that infants’ experience withopening drawers may play a role in whether or not they compensate in theiranticipatory adjustments for the resistance accompanying a pull. In the motorexperience questionnaire, we asked parents if their infants had experience withopening drawers, and if so, how much. From 33 of the 34 participants, we col-lected estimates of such experience and established three groupings for thesample. The low experience group (n = 11) consisted of those infants for whomparents reported no or fewer than 4 weeks of drawer opening experience. Themoderate experience group (n = 13) consisted of those infants for whom par-ents reported between 4 and 12 weeks of drawer opening experience. The highexperience group (n = 7) consisted of those infants for whom parents reported14 or more weeks of drawer opening experience. As Figure 5 depicts, in bothlow and moderate experience groups, mean muscle force estimates for the227-g and 454-g weight conditions were virtually identical (low: M = 1.67,SD = 2.14, and M = 1.68, SD = 1.72, respectively; moderate: M = 3.44,SD = 3.30, and M = 3.81, SD = 2.74). For the high experience group, in con-trast, the muscle force estimates for the 227-g condition (M = 1.79, SD = 1.46)differed significantly from the muscle force estimates for the 454-g condition(M = 3.64, SD = 2.63), t(6) = –3.17, p < .05. Thus, infants with more than 3months of drawer opening experience responded to an increase in the resist-ance accompanying drawer openings with higher magnitude anticipatory pos-tural adjustments than infants with fewer months of drawer opening experienceor with no experience of drawer opening. Adjusting the magnitude of anticipa-tory postural activity to compensate for changes in the resistance accompany-ing a pull seems linked to specific experience with pulling action, rather thangeneral age-related changes.

DISCUSSION

Results of this study suggest that, over the period of 10 to 17 months, infantsincreasingly utilize anticipatory postural adjustments to support their pullingbehavior. Both the consistency with which infants employ anticipatory posturaladjustments in support of pulling behavior and the temporal specificity of theiranticipatory activity progressively improved between 10 and 17 months. By con-trast, infants’ anticipatory activity during this period seemed relatively insensitiveto the specific external resistance demands involved in a pulling task, with theexception of responding at 15 months.

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More specifically, anticipatory activity was present at 10 and 11 months, but itwas very inconsistent. In this age period, when infants in our sample were justbeginning to stand independently, less than one third of the infants’ pulls were ini-tiated within 240 msec of pull onset. In contrast, by 16 to 17 months, when 5 of 6infants had 3 or more months of walking experience, over half of infants’ pulls in-volved anticipatory activation within 240 msec of pull onset. Even at 10 and 11months, however, more temporally diffuse anticipatory adjustments did notpredominate. In fact, prior to 16 months, when infants engaged in prospectivepostural activity, they employed both temporally specific and temporally diffuseactivations. Both forms were present throughout the age period under investiga-tion, but by 16 to 17 months, temporally specific anticipatory adjustments hadbegun to predominate. When we consider both forms of postural adjustmentjointly, that is, activity initiated within 500 msec of pull onset, close to two thirds

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FIGURE 5 Mean muscle force estimates (+SE) for each of three levels of drawer openingexperience. Low = no or fewer than 4 weeks of experience, moderate = between 4 and 12 weeksof experience, high = 14 or more weeks of experience.

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of the pulls performed by the 13-month-olds and over three fourths of the pullsperformed by the 16- to 17-month-olds involved prospective control.

Contrary to our hypothesis, bilateral anticipatory postural adjustments did notpredominate at early ages, to be replaced by unilateral adjustments later in devel-opment. Rather, unilateral anticipatory activity was more common in generalacross all ages, with exceptions at 13 and 16 to 17 months. Two noteworthy trendreversals between 13 and 15 months occurred: a marked increase in unilateral an-ticipatory activity, following a decrease prior to 13 months, and a marked decreasein bilateral anticipatory activity, following an increase from 10 to 13 months. If wecompare the standing experience of 13-month-olds (M = 6.33 weeks, SD = 3.67)with that of infants at 14 months (M = 12.5 weeks, SD = 8.54) and at 15 months(M = 13.33, SD = 6.89), we can see that 13-month-olds are only beginning to con-solidate their independent stance, in contrast to 14- and 15-month-olds. Infants at13 months also have next to no walking experience (1 infant had 4 weeks of walkingexperience, 3 had less than 2 weeks, and 2 had no walking experience), in contrastto the majority of infants at 14 and 15 months. Thus, infants may rely on bilateralanticipatory activity to a greater degree at 13 months than at 14 and 15 months.This makes sense from the assumption that a bilateral activation of posturalmuscles is a more stable procedure, producing a more articulated and redundantoutput. Thus, if children are less sure about their postural stability, they shouldpreferably produce bilateral activation. By 14 and 15 months, unilateral anticipa-tory activation may be sufficient to ensure stability.

In line with Forssberg et al.’s (1992) findings regarding the lack of anticipation ofthe weights of lifted objects, most infants between 10 and 17 months did not adjustthe magnitude of their anticipatory postural activity to compensate for differences in the resistance of the drawer to their pulling actions. In fact, only 15-month-oldscompensated for weight condition differences with magnitude difference in their an-ticipatory postural adjustments. However, grouping infants in terms of their experi-ence with opening drawers revealed a more systematic developmental trajectorysuch that infants with more than 3 months of drawer opening experience adjustedtheir anticipatory postural activity in accordance with weight condition differences,but those with less or no experience did not. Thus, as infants gained experience withopening drawers, they started to account for differences in the resistance accompa-nying a pull by changing the magnitude of their anticipatory postural adjustmentsaccordingly.

In general, our results accord with the view that anticipatory postural adjust-ments accompany action to some degree even in the early developmental stages ofacquiring new postural frameworks. Specifically, infants in our study showedsizeable, progressive increase in prospective control of upright stance between 10and 17 months, when infants are learning to stand and walk independently. Antic-ipatory postural adjustments in infants 13 months and older were consistentlypresent in some form, at a point in our sample when all infants were gaining

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independent standing experience and many were in the earliest stages of inde-pendent walking. This study thus complements the work of von Hofsten andWoollacott (1990) showing prospective postural control of seated reaching ininfants at 9 months, when infants are well coordinated in independent sitting.However, from the standpoint of age differences in general, our results also accordwith the work of van der Fits et al. (1999). Specifically, van der Fits et al. identi-fied the period between 12 and 15 months as one of transition between inconsis-tent and consistently present prospective control of seated reaching, with infantsdisplaying anticipatory activity in fewer than 30% of trials at 6, 8, 10, and 12months but in a little over half of their trials at 15 months (primarily in the neckextensor muscles). These data closely mirror the proportional data we report forspecific APA, as Figure 3 attests, despite differences in the postural muscles andposture-movement conditions sampled.

Although not designed to address discrepancies between von Hofsten andWoollacott (1990) and van der Fits et al. (1999), this study nonetheless raises in-triguing questions when considered in light of this seated reaching research. Giventhe high degree of correspondence in developmental trend between our work andthat of van der Fits et al., we ask: Does the period of 13 to 15 months usher in a tran-sition in the consistency and temporal specificity with which anticipatory posturaladjustments are employed irrespective of any specific postural framework? In otherwords, does this period of development involve a broad transition in postural con-trol, reflecting not just the emergence of prospective control in upright stance butalso in independent sitting and other postural frames? Or does the development ofprospective control involve multiple instantiations so that whenever infantsdevelop a new form of balance, concomitant developments in anticipatory posturaladjustments specific to the posture in question will arise? Developmental change inanticipatory postural adjustments may, in fact, be specific to a given posturalframework, such that prospective postural control of seated action follows an en-tirely different developmental course from that of prospective control in uprightstance. Without additional research on prospective activity during seated reaching,both questions reflect viable developmental accounts for anticipatory postural con-trol in infancy.

In their longitudinal study of postural control during upright stance, Barelaet al. (1999) reported a transition from reactive to prospective use of a contact sur-face for maintaining balance once infants had begun to master independent walk-ing. Notably, this transition occurred between approximately 12 and 13.5 months;thus, our finding of consistent anticipatory postural activity from 13 monthsonward underscores the results of Barela et al. Regrouping our age data in termsof infants with and without independent walking experience (4 or more weeks ofexperience vs. no experience or less than 2 weeks) reveals significant, marked in-creases in the temporal specificity and consistency of anticipatory postural adjust-ments as infants gain experience with walking. Once infants in our sample began

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walking by themselves, a little over half of their pulls involved anticipatoryadjustments in the G muscle within 240 msec of pull onset, in contrast to roughly30% of the pulls from samples without independent walking experience. Thus,our data, like those of Barela et al., highlight the emergence of independent walk-ing as a potentially significant transition point for the development of prospectivestance control (see also van der Fits et al. [1999] for possible links between walk-ing onset and prospective control of seated reaching).

Linking independent walking to the development of anticipatory postural con-trol is also consistent with work chronicling relations between motor developmentand reactive postural control in infancy. Hadders-Algra and colleagues (Hadders-Algra, Brogren, Apel, & Forssberg, 1994; Hadders-Algra, Brogren, & Forssberg,1996), for example, daily trained a group of infants from 5 to 10 months of age forbalance control and found that it accelerated the development of postural controlin a significant way. In addition, Sveistrup and Woollacott (1996) reported signif-icant increases in the consistency of postural muscle activation after balanceperturbations once infants began walking independently. With the transition fromindependent standing to independent walking, infants on a regular basis face thedemanding task of maintaining balance while moving the standing body forward.Consequently, the context of walking readily affords extended opportunities forinfants to establish predictive strategies for ensuring postural stability underdestabilizing conditions. Independent walking experience may thus provide aglobal foundation for the consolidation of anticipatory postural adjustmentsduring standing that is not specific to pulling behavior per se but to conditions ingeneral that threaten the stability of maintaining a fully vertical posture (see stud-ies by Bril & Breniere [1991, 1992] to support this conjecture).

Considerable caution must be exercised, however, when viewing our results,those of Barela et al. (1999), and those of van der Fits et al. (1999) from the stand-point of transitions in motor development, as testing age is confounded with stand-ing and walking experience in all of this research. Thus, designing research to sys-tematically disentangle the effects of walking experience from the effect of age ofonset for walking is a critical next step for the investigation of prospective posturalcontrol in infancy. Studies detailing the influence of crawling experience on cognitive,social, and emotional development are instructive in this regard (e.g., Bertenthal,Campos, & Barrett, 1984; Campos, Bertenthal, & Kermoian, 1992; Kermoian &Campos, 1988). Further investigations of prospective control could, for example,involve holding infant age constant while examining variations in walking experi-ence. In an especially cogent design, Barrett and Campos (1983) crossed durationof crawling experience with age of onset for crawling by contrasting the effect of11 versus 41 days of experience in infants who began crawling at different ages(6.5, 7.5, and 8.5 months). Such a design could be used to study development inboth independent standing and walking as they relate to prospective posturalcontrol. Studies of this nature are needed to raise arguments regarding the role of

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independent walking in the development of anticipatory postural adjustmentsabove basic speculation.

In summary, these results demonstrate progressive developmental change be-tween 10 and 17 months in infants’ prospective control of standing balance. Al-though anticipatory postural adjustments during pulling behavior are present onoccasion in infants under 13 months of age, they become much more consistentand temporally specific thereafter. In addition, experience with opening drawerscoincides with changes in infants’ anticipatory compensation for different resist-ances to pulling behavior.

ACKNOWLEDGMENTS

This research was supported by grants from the National Institutes of Health (HD16195) and the National Science Foundation (SBE 9704764) to Bennett I. Bertenthal.David C. Witherington was supported by National Insititute of Child Health and Human Development postdoctoral training grant HD 07323. Claes von Hofsten alsoreceived support from the Bank of Sweden Tercentenary Foundation, and MarjorieH. Woollacott was supported by National Science Foundation grant 202300.

We thank the parents and infants who participated in this study. We are alsoindebted to Dr. David N. Lee, who came up with the cabinet idea.

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