Changes in posture control across the life span - a systems approach.

Changes in Posture Control Across the Life Span--A Systems Approach An analysis of the behavioral changes occurring during the acquisition of independent stance shows that infants begin to stand with help at about 8 to 9 months of age, begin to walk with help at 11 months, pull themselves to a standing position at about 12 months, stand alone at 14 months, and walk alone at about 15 months of age. [1,2] It is widely noted that in the first few months of walking, the infant steps with a wide base and the arms raised. Walking characteristics gradually change over the next few years, becoming adultlike by about 5 to 7 years of age.

What neural mechanisms underlie the predictably changing patterns of behavior seen in infants learning to stand and walk independently? Two models of central nervous system (CNS) control--the reflex-hierarchical model and the systems model--have been used to describe the neural basis for developing posture and movement control in children. In the reflex-hierarchical model, the CNS is hypothesized to be organized as a strict vertical hierarchy. In this ascending hierarchy, primitive reflexes such as stretch reflexes are controlled at the spinal cord level, with the asymmetric tonic neck, symmetric tonic neck, and tonic labyrinthine reflexes being controlled by the next higher level, the brain stem. The righting reactions, a group of reactions responsible for maintaining alignment to gravity and keeping body parts in alignment after rotation, are controlled at a slightly higher CNS level, the midbrain. [3,4]

Equilibrium reactions, described as the body's response to tilting of the support surface, are hypothesized to be controlled by the highest level of the CNS, the cortex. [5,6] Higher-level equilibrium reactions, as described by Weiss, [5] are purported to be elicited by stimulation of the labyrinth; however, this explanation ignores the contribution of visual and somatosensory components to equilibrium control.

Researchers who have taken a reflex-hierarchical approach have hypothesized that voluntary movement control is achieved either through the inhibition of the more primitive reflexes by cerebral cortical pathways [7] or through reflexes that become the substrata for voluntary actions. [8] The model predicts that prior to attaining the next developmental milestone, equilibrium reactions must mature in the previous milestone. Thus, before children can sit, they must first have developed mature equilibrium reactions in the prone position; prior to standing, equilibrium reactions must be present in the sitting and quadruped positions. [4,6,9]

In summary, in the reflex-hierarchical model, motor development is viewed as moving from reflexive to voluntary control as the child matures. In addition, the emergence of independent balance and locomotion is seen as dependent on the maturation of sequentially higher levels of the CNS hierarchy, with higher levels of behavior, such as the equilibrium reactions, modifying immature behaviors such as tonic reflexes, controlled by lower levels within the CNS. [10]

Many therapeutic techniques used in rehabilitation of balance disorders are based on assumptions regarding the importance of normal reflex maturation to development. For example, neurodevelopmental treatment suggests positions and movements designed to inhibit primitive reflexes, such as bilateral midline activities designed to inhibit the asymmetric tonic neck reflex. [11,12] Pediatric assessment techniques relying on a reflex-hierarchical model attempt to determine a developmental level using both reflex tests (spinal reflexes, brain-stem reflexes, midbrain reflexes) and tests of voluntary control. For example, developmental protocols such as those of Chandler et al, [3] Milani-Comparetti and Gidoni, [6] Fiorentino, [13] and Brazelton [14] were created to provide a systematic approach to evaluating essential parameters of function in children, including muscle tone, primitive reflexes, automatic reactions, and voluntary movements. A potential explanation for lack of balance control would be the presence of primitive reflexes that constrain the emergence of more mature higher-level righting and equilibrium reactions. Treatment of a child with developmental delays would focus on sensorimotor techniques that progress the child through successively higher levels of reflexes and reactions.

A more recent model of motor control is the "systems," or "distributed control," model that evolved from the work of Bernstein. [15] In systems theory, the body is modeled as a mechanical system with mass that is subject to gravity and inertial forces. Because these factors change as we move, the same motor program gives different movements depending on the position we are in. Bernstein's model asks questions about the organism as an active agent in a continuously changing environment. He thus explored the physiology of activity, not reactions.

It was also Bernstein [15] who first brought forth the idea of synergies as muscles that are constrained to act as a unit. He viewed the synergy as a way for the nervous system to solve the control problem of coordinating many joints as part of a single movement, and he gave examples of possible synergies such as those found in locomotion, postural control, and breathing.

According to the systems model, the nervous system is seen as part of a flexible complex of systems and subsystems sharing in the control process. Thus, movement is always an emergent property that comes from the complex interactions of these systems.

Development of

Posture Control--A

Systems Perspective

Our experimental approach to studying the development of balance control in children relies on the systems model. In the following sections, we will introduce some of our basic concepts related to the study of balance development from a systems perspective and present results from research on developmental changes in components of postural control underlying the emergence of independent mature balance control.

A fundamental hypothesis in our work is that the development of independent stance and locomotion emerges from an interaction among multiple neural and mechanical components contributing to balance control. We hypothesize that certain critical components are rate-limiting in the development of balance and gait. Rate-limiting components are those aspects of the system that limit the rate at which the independent behavior emerges. Thus, the emergence of independent stance must await the maturation of the slowest critical component. Experimental studies examining the development of balance control in healthy children suggest the following nervous system and musculoskeletal components may contribute to the emergence of independent stance and locomotion: postural muscle response synergies for controlling balance; visual, vestibular, and somatosensory systems for detecting loss of balance; adaptive systems for modifying sensory and motor systems to changes in task or environment; muscle strength; joint range of motion; and body morphology. [7,15-19] Current studies are examining the relative influence of each of these components on the emergence of independent stance and locomotion. [20]

The systems model suggests that multiple neural and biomechanical factors interact to achieve the goal of balance. The task of balance requires that the center of body mass be maintained over the base of support. A cone has been used to represent the task of upright balance because, for a subject standing with feet together on a normal flat surface, the area of stability resembles that of a cone-shaped structure, with its base originating at the base of support. [16] The cone represents a set of equivalent positions, that is, all the points from which you can return to a point of origin without taking a step or otherwise moving your base of support. [16,21] The "stability cone" is the domain of stable movement for a particular postural task, the edges of which are the outer bounds of equilibrium for the task. [16] The following sections present results from research exploring developmental changes in components of postural control.

Musculoskeletal and Body

Morphology Changes

In healthy adults, limits of stability are determined by mechanical constraints that include those from both the individual (eg, height and foot length, strength, and ROM) and the environment (eg, type and consistency of the support surface). [21] How do rapidly changing musculoskeletal and body morphology characteristics affect the development of stability in children? We hypothesize that, because of differences in body morphology (eg, height, center of mass, foot length), the boundaries of individual stability cones will vary and that this variability will affect the selection of motor strategies appropriate to maintaining the body within the boundaries of the cone. [16] For example, previous research [21-23] has identified three postural movement strategies that are typically used by healthy adults for controlling balance: (1) the ankle strategy, in which balance adjustments are made at the ankle joint and the individual sways as an inverted pendulum; (2) the hip strategy, in which adjustments are made predominantly at the hip; and (3) the suspensory strategy, in which the subject flexes at the ankle, knee, and hip to lower the center of gravity toward the base of support.

The efficiency of a particular strategy, however, depends on a number of characteristics. For example, McCollum and Leen [16] have indicated that the movement of an inverted pendulum is characterized by a time constant that indicates the rate of fall from an upright position. The time constant is the inverse of the natural frequency of a pendulum, and the shorter the pendulum, the faster its natural frequency. A typical adult has a time constant for a single oscillation of 1.92 seconds, with a quarter cycle (the time to go from upright to the limits of stability) of 480 milliseconds. Because an adult's muscle response times for the ankle strategy are in the order of 100 milliseconds, he or she can easily respond to external threats to balance. According to McCollum and Leen, [16] the time constant for balance involving movement at the hip is shorter than that for the ankle, because a two-link pendulum is being modeled. In this case, a quarter cycle is 173 milliseconds. However, the onset of muscle responses for a hip strategy is between 73 and 110 milliseconds. [23] Thus, the adult can still use this strategy with a reasonable safety margin.

However, because of infants' shorter height, McCollum and Leen [16] predict that 1-year-old infants will have a quarter-cycle time of 333 milliseconds. Their ankle muscle responses are typically activated at 100 to 125 milliseconds, which is still within an effective range for regaining balance, if it is perturbed. An infant's hip movement, however, would have a quarter-cycle time of 114 milliseconds and thus would complete a quarter cycle too quickly to be corrected. As a result, they predict that a hip strategy would not be seen in young children. Thus, the changes in height that occur during an infant's or a toddler's development are examples of musculoskeletal changes that may contribute to the emergence of stability.

Changes in Muscle

Response Synergies

Hartbourne et al [17] performed a longitudinal study on the development of muscle activation sequences associated with independent sitting in children aged 2 to 5 months. Children were first supported around the trunk by the experimenter, then released to sit on their own, during which time they slumped forward. Electromyographic (EMG) data were collected from muscles of the back and hip. The authors noted that trunk displacement significantly decreased between 2 to 3 and 4 to 5 months of age.

Hartbourne et al [17] also noted that children in stage 1 (age 2-3 months), who were unable to sit independently, showed great variability in the order of muscle activation, both within and across subjects. Children in stage 2 (age 4-5 months) showed an emergence of a distinctive order of muscle response organization, with each child showing a preferred pattern or synergy. The most frequent patterns seen were: lumbar paraspinal-hamstring muscles, lumbar paraspinal-quadriceps femoris muscles, and hamstring-quadriceps femoris muscles, with the lumbar paraspinal-hamstring and hamstring-quadriceps femoris muscle synergies associated with the least trunk displacement. Hartbourne et al [17] concluded that the postural synergies that aid in postural control while sitting develop over time (with each child developing a preferred synergy). Because the study was longitudinal in nature, it also gives a window for observing the gradual emergence in each child of a preferred muscle response synergy.

Recent studies in our own laboratory on the development of neuromuscular response organization underlying postural control in seated infants 4 to 14 months of age have attempted to determine the time course of the development of postural muscle response synergies used in response to external threats to balance. [18] In these experiments, the infant was placed in an infant seat or seated independently on a support surface (a hydraulically activated platform) that could be moved forward or backward. Surface EMGs were used to monitor the responses of the neck extensors and flexors, the trunk extensors, and the abdominal muscles.

We found that infants aged 5 to 6 months, who could not yet sit independently, showed responses only in the muscles of the neck. When the platform was moved backward and the child swayed forward, the neck extensor muscles were activated to compensate for the sway. Postural response synergies of independently seated 8- to 14-month-old children included muscles of both the neck and trunk and were directionally specific to compensate for the platform-induced sway. Thus, when the platform moved backward, causing forward sway, the trunk extensor and neck extensor muscles were activated, and, when the platform moved forward, causing backward sway, the trunk flexor and neck flexor muscles were activated.

A cross-sectional study [18] using the same platform system to study posture control in the developmental transition period leading to independent stance (Fig. 1) has examined infants in a range of stages in learning to stand, from no experience in independent stance at 8 months, through minimal experience at 10 months, to 6 weeks' experience in stance and walking at 14 months. The 8-month-old infant (lightly supported at the waist, to maintain stability) showed no muscle responses to platform movements. These results could lead to the assumption that lack of nervous system maturity or experience caused this lack of response; however, it is also possible that the support given by the mother reduced the effect of the platform movement or the need for a postural response.

For the 10-month-old infant, who was standing but not walking independently, directionally specific responses were observed in the distal muscle of the leg (gastrocnemius) during 40% of the platform movements causing anterior sway. Hamstring muscle responses were observed in only one trial.

For the 14-month-old infant, who was walking independently, directionally appropriate leg muscle responses with adultlike response organization were observed consistently. When the platform was moved backward, the infant showed forward sway, and the gastrocnemius (distal) and hamstring (proximal) muscles responded in an ascending sequence in which the center of mass returned to its normal range. Gastrocnemius muscle responses in the 14-month-old infant were at latencies close to those seen in adults (109[+ or -]24 milliseconds). Thus, this gradual emergence of postural response organization in children learning to stand is similar to that seen by Hartbourne et al [17] and Woollacott et al [18] in children learning to sit. In each study, an increase in neuromuscular response organization was observed with age and experience with the new skill.

Although adultlike response organization in the infant has been observed within 6 weeks of experience walking, there are still many response characteristics that are immature. For example, Forssberg and Nashner [24] observed that responses of children aged 1 to 3 years were slower and more variable than those of adults and showed more antagonist muscle coactivation. As in the model of McCollum and Leen, [16] slower EMG responses and faster rates of sway acceleration were seen in young children as a result of their shorter stature. These outcomes caused larger and more oscillatory sway amplitudes than Forssberg and Nashner [24] observed in older children and adults.

Shumway-Cook and Woollacott [25] showed that responses of 15- to 31-month-old children were consistently large in amplitude and longer in duration when compared with older children and adults (Fig. 2). An unpredicted change in response characteristics in the 4- to 6-year-old age group was also noted. A regression was apparent in the postural response organization in the 4- to 6-year-old children in that their synergies were more variable and longer in latency than in the 15-month- to 3-year-old children, the 7- to 10-year-old children, or the adults (Fig. 2). The 4- to 6-year-old group was more variable in muscle response characteristics than the 15-month- to 3-year-old children; however, behavioral data indicated that they swayed less in response to platform movements. [25] By the age of 7 to 10 years, this variability was greatly reduced, and this age group exhibited postural responses that were essentially like those seen in the adult synergy (Figs. 2C, 2D). Thus, children go through a transition period at 4 to 6 years of age in which their responses become slower and more variable, followed by maturation of the responses at about 7 to 10 years of age.

Developmental Changes

in Sensory Inputs for

Posture Control

In addition to these motor strategies for posture control, a number of sensory strategies are available to aid in balancing. Thus, a child or adult may create different rules for combining the use of the available sensory inputs depending on the environmental circumstances. Normally, three classes of sensory inputs are available for balance control: (1) somatosensory inputs, (2) visual inputs, and (3) vestibular inputs. It has previously been shown that healthy adults rely primarily on somatosensory inputs under normal sensory conditions in which all sensory inputs are available. [26] However, they can be made to rely on visual inputs by giving them a novel stance condition or by making support-surface inputs unreliable (eg, by standing on a narrow beam). [27]

Lee and Aronson [19] have shown that children learning to stand initially are more influenced by visual cues than are adults. Owen and Lee [28] hypothesize that this initial high susceptibility to incongruent visual information is due to the infant having poorer information from the ankles and feet than the adult, because the infant has not yet had the opportunity to calibrate or fine-tune this information for use in balance control. With practice in independent stance and walking, this calibration takes place and the infant relies less on visual cues.

Another experimental paradigm [29] that has been used to test the ability of children to use different sensory inputs and to adapt to altered sensory conditions requires the child to stand quietly for 5 seconds under conditions in which the redundancy of sensory inputs relevant for balance control is gradually reduced until only vestibular inputs remain. The conditions include (1) somatosensory ankle joint, visual, and vestibular inputs normal; (2) somatosensory ankle joint and vestibular inputs normal, eyes closed; (3) ankle joint inputs minimized by rotating the platform in direct relationship to body sway, but visual and vestibular inputs minimized (as above), eyes closed, vestibular system normal.

In studies by Forssburg and Nashner [24] and Shumway-Cook and Woollacott, [25] the performance of children under these conditions was measured by determining body sway as a percentage of theoretical maximum sway, with 100% indicating loss of balance. This procedure allows the comparison of balance abilities in children of different heights. Shumway-Cook and Woollacott [25] indicated that even under normal stance conditions, 4- to 6-year-old children swayed significantly more (Fig. 3, far left) than older children or adults (the youngest children could not tolerate the altered conditions without crying). With eyes closed, the stability of the 4- to 6-year-old children decreased further, yet all of them were able to remain within their limits of stability (Fig. 3). However, in the condition in which the support surface was rotated with body sway, thus keeping the ankle joint at 90 degrees and eliminating sway-related ankle joint inputs, the 4- to 6-year-old children were greatly destabilized and one lost balance (Fig. 3). The last sensory condition, with ankle joint inputs unrelated to sway and with eyes closed, leaving primarily vestibular cues to aid in balance, was the most difficult. Four of the five children in this age group needed assistance to maintain stability, whereas none of the older children or adults lost balance (Fig. 3, far right).

An interesting observation by Forssberg and Nashner [24] is that when the youngest children balanced under conditions in which the support surface and the visual environment were rotated with body sway to remove sway-related inputs, the youngest age group showed long delays between the beginning of forward sway and the activation of the appropriate gastrocnemius muscle. They noted that the children then began to sway backward, but this time activated the appropriate tibialis anterior muscle response only when beyond the limits of stability. They noted that postural responses were activated much more quickly in 7- to 10-year-old children and that oscillations remained within normal limits.

These studies suggest that children under 7 years of age are unable to balance efficiently when both somatosensory and visual cues are removed, leaving only vestibular cues to control stability. Shumway-Cook and Woollacott [25] found that 4- to 6-year-old children showed progressively decreasing stability as they lost redundant sensory inputs for postural control. This age group also was less efficient than older children at shifting from the use of ankle joint somatosensory cues to visual cues when ankle joint inputs were made incongruent with body sway. This finding may indicae the inability of 4- to 6-year-old children to resolve intersensory conflict during postural control.

Integration of Posture Control

Into the Gait Cycle

Berger et al [30] studied children who walked on a treadmill and examined their ability to integrate postural responses into the step cycle. Responses were evoked by momentarily accelerating or decelerating the treadmill speed during the step cycle.

Results indicated that monosynaptic reflexes were present in the youngest children (1 year old), diminished in amplitude in 2.5-year-old children, and absent in 4-year-old children and adults. Postural responses also became shorter in duration and showed less antagonist muscle coactivation as the children developed. The results of this study were similar to those reported previously (ie, both a shortening in the duration of postural responses during development and a reduction in the coactivation of antagonist muscles along with the agonist muscles). The monosynaptic reflexes were observed in addition to the longer-latency automatic postural responses. It is of interest that the children showed a gradual reduction in amplitude and disappearance between the ages of 1 and 4 years, as the postural responses began to show more mature characteristics.

Aging and Balance Control

Studies in our own laboratory have used the systems approach to expand the study of balance control to the entire life span in order to determine the specific changes in the different nervous system and musculoskeletal components contributing to balance control. The following sections will summarize changes in the different subsystems in the elderly.

Muscle Response Synergies

Woollacott et al [31] and Manchester et al [32] have investigated whether there are age-related changes in the ability to appropriately activate and organize postural muscle synergies when exposed to threats to balance. Woollacott et al [31] compared the muscle response characteristics of 12 older adults (61-78 years of age) with those of 14 younger adults (19-38 years of age), using the platform translations described previously. They noted that the automatic postural responses of the older adult group showed the following changes in both timing and amplitude characteristics when compared with the young adults:

1. Significant increases in the absolute latency of distal (ie, tibialis anterior) muscle responses in response to platform translations causing posterior sway (onset latencies: young adults, 102[+ or -]6 milliseconds; older adults, 109[+ or -]9 milliseconds). Figure 4 shows the EMG responses of young and older adults to a platform perturbation, giving examples of the response delays seen in the older adults.

2. Intermittent reversals in the normal distal-to-proximal sequence of leg muscle contractions so that the proximal quadriceps femoris muscle was activated before the distal tibialis anterior muscle. Five of the 12 older subjects showed these intermittent reversals (Fig. 4C).

3. A larger incidence of short-latency spinal monosynaptic reflexes, when subjected to platform rotations. Seven of the 12 older adults showed an activation of monosynaptic reflexes, whereas none of the younger subjects showed this activation. However, the incidence of these reflexes was small (18% of the trials), even in those subjects in which they were elicited. Manchester et al [32] also found that older adults coactivated antagonist muscles with the agonist muscle significantly more than did young adults when responding to platform translations.

Sensory Inputs Contributing to

Posture Control

Woollacott et al [31] also tested the ability of older adults to retain stability under conditions of reduced or conflicting information from the visual, vestibular, and somatosensory systems. The protocol required that the older and younger adult groups balance for a 10-second period under six different sensory conditions: (1) normal vision, normal base of support; (2) eyes closed, normal base of support; (3) visual environment rotated to follow body sway, normal base of support; (4) normal vision, base of support rotated to follow body sway; (5) eyes closed, base of support rotated to follow body sway; and (6) vision and base of support rotated to follow body sway. The last two conditions reduced both relevant visual and somatosensory cues for posture control, so that primarily vestibular cues remained. They found that the sway measurements of the older adults were not significantly greater than those of the young adults for the first four sensory conditions. However, for the last two conditions, the older adults had significantly more sway than the young adults, and many of the older adults lost stability, requiring assistance to regain their balance. Two of the older adults lost balance under condition 5, and 6 of the 12 older adults lost balance under condition 6.

According to the systems model, these results indicate that postural control is an emergent property that involves the interactions of a number of sensory systems. The results show that as long as two sensory inputs are available, both young and older adults can easily shift from the use of one sensory input to another. However, when only one sensory input--the vestibular system--remains, the sway of the older adult is sufficiently impaired to cause loss of balance in many instances.

Musculoskeletal Changes

An additional body system that contributes to balance control is the musculoskeletal system, and one characteristic of the musculoskeletal system--muscle strength--decreases significantly with age. [33-35] Whipple et al [35] found that elderly nursing home residents with a history of falls had severe impairments in overall ankle muscle strength when compared with age-matched controls. They noted that ankle dorsiflexion strength was most severely impaired in these nursing home residents with a history of falls. These data are similar to those reported by Woollacott et al, [31] which showed a significant slowing in onset latency for the tibialis anterior muscles in response to external threats to balance.

Summary and Conclusions

These studies on the development of posture control across the life span and its integration with voluntary tasks such as walking show a number of interesting principles of developmental progression. First, infants show a clear cephalocaudal gradient in the development of postural responses, with control first appearing in the muscles of the neck, then the trunk, and finally the legs. Data show that postural muscle synergies develop appropriate temporal organization through experience in each new level of postural skill development. Muscle strength changes may also contribute to the development of postural control, but few data are available on this aspect of postural development. We believe sensory inputs contributing to posture control may be able to influence postural responses very early in development, with postural responses being evident if influenced by vision alone, or by somatosensory and vestibular cues in isolation.

Studies on the older adult indicate small, but significant, increases in the onset latencies and disruptions in the temporal organization of postural muscle responses when subjects are given external threats to balance. In addition, older adults, like young children, use antagonist muscles more often in coactivation with agonist muscles when balancing. [31]

Older adults also have more difficulty balancing when sensory inputs contributing to balance control are reduced, so that they have less redundancy of sensory information. Thus, when both somatosensory and visual inputs are made incongruent with postural sway, the older adult shows significantly increased sway compared with the young adult, and many older adults lose balance completely. This characteristic is also similar to that seen in young children. Muscle (ie, ankle dorsiflexor) weakness may also be a factor in balance dysfunction in the older adult.

Given the many similarities in functional capabilities of the different systems contributing to balance control in the child and the older adult when compared with the young adult, do these results support the strict vertical hierarchy hypothesis that as children mature, higher nervous system centers take over function from more primitive reflex systems, and that as adults age and higher centers deteriorate, lower-level systems begin to show functions that reemerge? Although there are limited data to show that there is some reemergence of spinal reflexes in the older adult, [36] all other similarities in function between the different musculoskeletal and nervous subsystems can be explained by developmental changes in functional status of each system independently. There is no need to invoke the existence of a strict vertical hierarchy. For example, the similarities in use of antagonist muscles along with agonists in posture control in the two age groups (children versus older adults) simply imply that each may use the agonist-antagonist coactivation to stiffen the ankle joint and thus limit the degrees of freedom needed for postural control. This is a typical strategy found in any motor skill when function is not optimal; it is not an indication of a "lower level" of the vertical hierarchy reemerging in dominance.

The systems model can be used to evaluate changes in the different systems contributing to balance control across the life span by asking questions such as: When the function of one system contributing to balance control is unavailable, what other systems can compensate? Are there specific environmental conditions that threaten balance control when specific systems are impaired, and can these conditions be avoided? and Can balance strategies be modified to improve balance function when a specific system is no longer functioning at optimal levels? Thus, this model has great flexibility and great potential in contributing not only to our understanding of balance changes across the life span, but to therapeutic interventions in the child or the older adult with balance dysfunction. However, our understanding of the clinical implications of many of the experimental findings has only recently been explored. [37,38] As a result, effective approaches to assessment and treatment of some types of postural problems identified through systems research are still limited.

M Woollacott, PhD, is Professor, Institute of Neuroscience and the Department of Physical Education and Human Movement Studies, Gerlinger Hall, University of Oregon, Eugene, OR 97403 (USA). Address correspondence to Dr Woollacott.

A Shumway-Cook, PhD, PT, is Director, Balance Disorders Program, Emanuel Rehabilitation Center, 3001 N Gantenbein, Portland, OR 97227.

References

[1] Shirley M. The First Two Years: A Study of Twenty-Five Babies. Minneapolis, Minn: University of Minnesota Press; 1931:1.

[2] McGraw MB. Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion. J Pediatr. 1940;17:747-771.

[3] Chandler LS, Andrews MS, Swanson MW. Movement Assessment of Infants: A Manual. Rolling Bay, Wash: Rolling Bay Press; 1980.

[4] Effgen SK. Integration of the plantar grasp reflex as an indicator of ambulation potential in developmentally disabled infants. Phys Ther. 1982;62:433-435.

[5] Weiss S. Studies in equilibrium reaction. J Nerv Ment Dis. 1938;88:153-162.

[6] Milani-Comparetti A, Gidoni EA. Routine developmental examination in normal and retarded children. Dev Med Child Neurol. 1967;9:631-638.

[7] Wyke B. The neurological basis of movement: a developmental review. In: Holt KS, ed. Movement and Child Development. Philadelphia, Pa: JB Lippincott Co; 1975:19-33.

[8] Twitchell TE. The automatic grasping responses of infants. Neuropsychologia. 1965;3:247-259.

[9] Haley S. Sequential analyses of postural reactions in nonhandicapped infants. Phys Ther. 1986;66:531-536.

[10] Gilfoyle EM, Grady AP, Moore KC. Children Adapt. Thorofare, NJ: Slack Inc; 1986.

[11] Bobath B, Bobath K. The neuro-developmental treatment. In: Scrutton D, ed. Management of the Motor Disorders of Children with Cerebral Palsy. London, England: Spastics International Medical Publications; 1984.

[12] Wat L. Mobility module counteracting the tonic labyrinthine reflex in a cerebral palsied child: suggestion from the field. Phys Ther. 1978;58:880-881.

[13] Fiorentino MR. Reflex Testing Methods for Evaluating CNS Development. Springfield, Ill: Charles C Thomas, Publisher; 1973.

[14] Brazelton TB. Neonatal Behavioral Assessment Scale. 2nd ed. Philadelphia, Pa: JB Lippincott Co; 1984.

[15] Bernstein N. Co-ordination and Regulation of Movements. New York, NY: Pergamon Press Inc; 1967.

[16] McCollum G, Leen TK. Form and exploration of mechanical stability limits in erect stance. Journal of Motor Behavior. 1989;21:225-244.

[17] Hartbourne R, Giuliani CA, NacNeela J. Kinematic and electromyographic analysis of the development of sitting posture in infants. Dev Med Child Neurol. 1987;29:31-32.

[18] Woollacott MH, Debu B, Mowatt M. Neuromuscular control of posture in the infant and child: is vision dominant? Journal of Motor Behavior. 1987;19:167-186.

[19] Lee DN, Aronson E. Visual proprioceptive control of standing in human infants. Percept Psychophys. 1974;15:529-532.

[20] Woollacott MH, Sveistrup H. Changes in sequencing and timing of muscle response coordination associated with developmental transitions in balance abilities. Human Movement Science. In press.

[21] Nashner LM, McCollum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci. 1985;9:135-172.

[22] Nashner L, Woollacott MH, Tuma G. Organization of rapid responses to postural and locomotor-like perturbations of standing man. Exp Brain Res. 1979;36:463-476.

[23] Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol. 1986;55:1369-1381.

[24] Forssberg H, Nashner LM. Ontogenetic development of postural control in man: adaptation to altered support and visual conditions during stance. J Neurosci. 1982;2:545-552.

[25] Shumway-Cook A, Woollacott MH. The growth of stability: postural control from a developmental perspective. Journal of Motor Behavior. 1985;17:131-147.

[26] Nashner LM, Berthoz A. Visual contribution to rapid motor responses during posture control. Brain Res. 1978;150:403-407.

[27] Lishman JR, Lee DN. The autonomy of visual kinaesthesis. Perception. 1973;2:287-294.

[28] Owen BM, Lee DN. Establishing a frame of reference for action. In: Wade MG, Whiting HTA, eds. Motor Development in Children: Aspects of Coordination and Control. Dordrecht, the Netherlands: Martinus Nijhoff/Dr W Junk Publishers; 1986.

[29] Nashner LM, McCollum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci. 1985;8:135-172.

[30] Berger W, Quintern J, Dietz V. Development of bilateral coordination of stance and gait in children. In: Amblard B, Berthoz A, Clarac F, eds. Posture and Gait: Development, Adaptation and Modulation. Amsterdam, the Netherlands: Elsevier; 1988:67-74.

[31] Woollacott MH, Shumway-Cook A, Nashner LM. Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev. 1986;23:97-114.

[32] Manchester D, Woollacott MH, Zederbauer-Hylton N, Marin O. Visual, vestibular and somatosensory contributions to balance control in the older adult. J Gerontol. 1989;44:118-127.

[33] Aniansson A, Hedberg M, Henning G, et al. Muscle morphology, enzymatic activity, and muscle strength in elderly men: a follow-up study. Muscle Nerve. 1986;9:585-591.

[34] Larsson L, Grimby G, Karlsson J. Muscle strength and speed of movement in relation to age and muscle morphology. J Appl Physiol. 1979;46:451-456.

[35] Whipple RH, Wolfson LI, Amerman PM. The relationship of knee and ankle weakness to falls in nursing home residents: an isokinetic study. J Am Geriatr Soc. 1987;35:13-20.

[36] Paulson G, Gottlieb G. Developmental reflexes: the reappearance of foetal and neonatal reflexes in aged patients. Brain. 1968;91:37-52.

[37] Shumway-Cook A, Horak FB. Assessing the influence of sensory interaction on balance: suggestion from the field. Phys Ther. 1986;66:1548-1550.

[38] Shumway-Cook A, Horak FB. Rehabilitation strategies for patients with vestibular deficits. Neurol Clin. 1990;8:441-457.