Transitions in Visual Proprioception: A Cross-Sectional Developmental Study of the Effect of Visual Flow on Postural Control

In the present study, a moving room paradigm was used that characterized the developmental progression of the effects of visual perturbations on stance control in subjects (N = 39) from 5 months to 10 years of age. Kinematic (probability of recording sway, magnitude of sway response) and electromyographic (probability and patterns of muscle activation, muscle onset latencies) data were found that suggested that visual flow simulating sway activates organized postural muscle responses and results in subsequent sway in standing infants as young as 5 months of age, well before they are able to stand independently. In new walkers, there was an increase in the magnitude of the effect of the visual perturbation, suggesting a possible increase in reliance on visual information. The magnitude of sway decreased to very low levels in older children and adults. The large-amplitude responses observed in the youngest age groups may indicate an inability to switch from an unreliable to a reliable source of perceptual information or an inability to modulate the responses produced following the perturbations. With increasing age and experience, the ability to resolve the conflict increased, with adult subjects demonstrating little sway response.     

Task demand effects on postural control in older adults

The literature shows conflicting results regarding older adults' (OA) postural control performance. Differing task demands amongst scientific studies may contribute to such ambiguous results. Therefore, the purpose of this study was to examine the performance of postural control in older adults and the relationship between visual information and body sway as a function of task demands. Old and young adults (YA) maintained an upright stance on different bases of support (normal, tandem and reduced), both with and without vision, and both with and without room movement. In the more demanding tasks, the older adults displayed greater body sway than the younger adults and older adults were more influenced by the manipulation of the visual information due to the room movement. However, in the normal support condition, the influence of the moving room was similar for the two groups. These results suggest that task demand is an important aspect to consider when examining postural control in older adults.     

Effect of visual surrounding motion on body sway in a three-dimensional environment

Unidirectional motion of a uniplanar background induces a codirectional postural sway. It has been shown recently that fixation of a stationary foreground object induces a sway response in the opposite direction (Bronstein & Buckwell, 1997) when the background moves transiently. The present study investigated factors determining this contradirectional postural response. In the experiments presented, center of foot pressure and head displacements were recorded from normal subjects. The subjects faced a visual background of 2 x 3 m, at a distance of 1.5 m, which could be moved parallel to the interaural axis. Results showed that when the visual scene consisted solely of a moving background, the conventional codirectional postural response was elicited. When subjects were asked to fixate an earth-fixed foreground (window frame) placed between them and the moving background, a consistent postural response in the opposite direction to background motion was observed. In addition, we showed that this contradirectional postural response was not transient but was sustained for the 11 sec of background motion. We investigated whether this contradirectional postural response was the consequence of the induced movement of the foreground by background motion. Although induced movement was verbally reported by subjects when viewing an earth-fixed target projected onto the moving background, the contradirectional sway did not occur. These results indicate that foreground-background separation in depth was necessary for the contradirectional postural response to occur rather than induced movement. Another experiment showed that, when the fixated foreground was attached to the head of the observer, the contradirectional sway was not observed and was therefore unrelated to vergence. Finally, results showed that the contradirectional postural response was, in the main, monocularly mediated. We conclude that the direction of the postural sway produced by a moving background in a three-dimensional environment is determined primarily by motion parallax.     

Development of postural stability limits: Anteroposterior and mediolateral postural adjustment mechanisms do not follow the same maturation process

There is increasing evidence that indicates a critical transition period for the maturation of postural control from the ages of 6–7 years. Some studies suggest that this transitional period may be explained by a change from a ballistic toward a sensory strategy, but the cause remains unknown. The purpose of this study was to investigate the influence of the transition period on dynamic postural control in a natural self-initiated leaning task under different sensory conditions. We evaluated the center of pressure (COP) displacement during maximum leaning in four directions (forward, backward, rightward, leftward) under three sensory conditions (eyes open, eyes closed and eyes closed standing on a foam). Three groups were tested: young children (4 years old), older children (8–10 years old) and adults (21–42 years old). The maximum COP excursion along the anteroposterior and mediolateral axes and the COP amplitude were analyzed. Young children showed smaller maximum anteroposterior and mediolateral COP excursion than other groups. Older children also exhibited a significantly smaller maximum excursion along the mediolateral direction but performed similar to adults along the anteroposterior direction. In a similar manner, the analysis of the COP amplitude did not indicate any differences between the groups along the anteroposterior axis. In contrast, along the mediolateral axis, the results showed developmental differences. Furthermore, the effect of sensory conditions was similar across the children's groups. Our results suggest an important plasticity period for the maturation of postural control mechanisms. Notably, our findings support the idea that the postural mechanisms controlling the anteroposterior axis reach maturity before the mechanisms involved in controlling the mediolateral axis.     

Locomotor experience affects self and emotion

Two studies investigated the role of locomotor experience on visual proprioception in 8-month-old infants. Visual proprioception refers to the sense of self-motion induced in a static person by patterns of optic flow. A moving room apparatus permitted displacement of an entire enclosure (except for the floor) or the side walls and ceiling. In Study 1, creeping infants and prelocomotor/walker infants showed significantly greater postural compensation and emotional responses to side wall movement than did same-age prelocomotor infants. Study 2 used true random assignment of prelocomotor infants to locomotor-training (via a powered-mobility device) and no-training conditions. Experimental infants showed powerful effects of locomotor training. These results imply that locomotor experience is playing a causal role in the ontogeny of visual proprioception.     

Deterministic and Stochastic Postural Processes: Effects of Task,Environment, and Age

Upright standing is always environmentally embedded and typically co-occurs with another (suprapostural) activity. In the present study, the authors investigate how these facts affect postural dynamics in an experiment in which younger (M age = 20.23 years, SD = 2.02 years) and older (M age = 75.26 years, SD = 4.87 years) participants performed a task of detecting letters in text or maintaining gaze within a target while standing upright in a structured or nonstructured stationary environment. They extracted the coefficients of drift (indexing attractor strength) and diffusion (indexing noise strength) from the center of pressure (COP) time series in anteroposterior (AP) and mediolateral (ML) axes. COP standard deviation decreased with drift and increased with diffusion. The authors found that structure reduced AP diffusion for both groups and that letter detection reduced younger SD _AP (primarily by diffusion decrease) and increased older SD _ML (primarily by drift decrease). For older and younger participants, ML drift was lower during letter detection. Further, in older letter detection, larger visual contrast sensitivity was associated with larger ML drift and smaller SD _ML, raising the hypotheses that ML sway helps information detection and reflects neurophysiological age.     

Visuomotor error augmentation affects mediolateral head and trunk stabilization during walking

Prior work demonstrates that humans spontaneously synchronize their head and trunk kinematics to a broad range of driving frequencies of perceived mediolateral motion prescribed using optical flow. Using a closed-loop visuomotor error augmentation task in an immersive virtual environment, we sought to understand whether unifying visual with vestibular and somatosensory feedback is a control goal during human walking, at least in the context of head and trunk stabilization. We hypothesized that humans would minimize visual errors during walking – i.e., those between the visual perception of movement and actual movement of the trunk. We found that subjects did not minimize errors between the visual perception of movement and actual movement of the head and trunk. Rather, subjects increased mediolateral trunk range of motion in response to error-augmented optical flow with positive feedback gains. Our results are more consistent with our alternative hypothesis – that visual feedback can override other sensory modalities and independently compel adjustments in head and trunk position. Also, aftereffects following exposure to error-augmented optical flow included longer, narrower steps and reduced mediolateral postural sway, particularly in response to larger amplitude positive feedback gains. Our results allude to a recalibration of head and trunk stabilization toward more tightly regulated postural control following exposure to error-augmented visual feedback. Lasting reductions in mediolateral postural sway may have implications for using error-augmented optical flow to enhance the integrity of walking balance control through training, for example in older adults.     

Anticipatory postural control in children

Postural responses, triggered by sensory feedback, are present very early in a child's development. The purpose of the present study was to investigate the ability of children to anticipate postural disturbances caused by self-initiated movements and their ability to coordinate anticipatory postural adjustments with movement execution. Children (N = 32) aged 4 to 14 years were asked to stand quietly on a stable force plate and to raise their right arm forward (or backward) to the horizontal position after a visual stimulus. Changes in the center of pressure beneath the feet were recorded before and during the arm raise. The anticipatory (feedforward) postural patterns seen before the arm movement, and noted in a previous study of adults, were present in the youngest of the children (4 years, 2 months). Longer reaction times and inconsistent postural responses (in the anteroposterior direction) suggest that children are less capable than adults of coordinating the anticipated postural adjustment with the forthcoming limb movement, however. In the lateral plane, anticipatory postural responses were initiated more consistently.     

Age Group Differences in Postural Adjustments Associated With a Stepping Task

In this study, differences among age groups in the postural adjustments associated with a stepping task were identified. Twenty subjects from each of 3 age groups, children (8-12 years), young adults (25-35 years), and older adults (65ndash73 years), performed the task in 2 movement contexts: place and step. In place, the subject simply lifted the foot and placed it on the step. In step, the subject lifted the foot, placed it on the step, and stepped up onto the step. Latencies of postural and focal muscle activation were determined by using surface electromyography and pressure switches. Center of pressure (CP) data were obtained by using a force platform. Subjects in all 3 age groups consistently demonstrated postural adjustments before movement initiation. Children displayed longer postural latencies than young adults as well as disproportionately large values for CP path length. Older adults showed prolonged postural-focal latencies and decreased CP excursions compared with the 2 younger age groups. These results suggest that maturation of coordination between posture and movement may not be fully complete in 8- to l2-year-olds and that increased restraint characterizes the performance of postural adjustments in healthy persons over 65 years of age.     

Anticipatory Postural Control in Children

Postural responses, triggered by sensory feedback, are present very early in a child’s development. The purpose of the present study was to investigate the ability of children to anticipate postural disturbances caused by self-initiated movements and their ability to coordinate anticipatory postural adjustments with movement execution. Children (N = 32) aged 4 to 14 years were asked to stand quietly on a stable force plate and to raise their right arm forward (or backward) to the horizontal position after a visual stimulus. Changes in the center of pressure beneath the feet were recorded before and during the arm raise. The anticipatory (feedforward) postural patterns seen before the arm movement, and noted in a previous study of adults, were present in the youngest of the children (4 years, 2 months). Longer reaction times and inconsistent postural responses (in the anteroposterior direction) suggest that children are less capable than adults of coordinating the anticipated postural adjustment with the forthcoming limb movement, however. In the lateral plane, anticipatory postural responses were initiated more consistently.     

Infants' coordination of auditory and visual depth information.

Using the preferential-looking procedure infants 5, 7, and 9 months of age were presented two videoimages side by side on separate monitors accompanied by a soundtrack that matched one of the images. Each infant was presented: (1) a stationary drum-beating toy paired with the same toy approaching and receding in depth, to assess infants' recognition both that changing sound amplitude is a property of an object that is moving in space and that constancy in amplitude is a property of a stationary object; (2) a drum-beating toy moving horizontally paired with one approaching and receding in depth, to assess infants' recognition that systematic increases and decreases in amplitude accompany object movement in a particular dimension, namely depth; and (3) two identical toys alternately approaching and receding in depth but out of phase (i.e., one approaching while the other is receding), to assess infants' recognition that increases and decreases in amplitude accompany a particular type of object movement in depth. Measures of mean duration of looking time indicated that the 5-month-olds looked reliably to the correct videoimage only for the stationary toy paired with the constant amplitude sound. The 7-month-olds recognized that changes in amplitude accompany object movement in depth but did not coordinate auditory with visual depth information as well as older infants. The 9-month-olds looked reliably to the correct videoimages in all conditions. Possible contributing factors to these developmental trends in performance are discussed.     

Perception of self-tilt in a true and illusory vertical plane

A tilted furnished room can induce strong visual reorientation illusions in stationary subjects. Supine subjects may perceive themselves upright when the room is tilted 90 degrees so that the visual polarity axis is kept aligned with the subject. This 'upright illusion' was used to induce roll tilt in a truly horizontal, but perceptually vertical, plane. A semistatic tilt profile was applied, in which the tilt angle gradually changed from 0 degrees to 90 degrees, and vice versa. This method produced larger illusory self-tilt than usually found with static tilt of a visual scene. Ten subjects indicated self-tilt by setting a tactile rod to perceived vertical. Six of them experienced the upright illusion and indicated illusory self-tilt with an average gain of about 0.5. This value is smaller than with true self-tilt (0.8), but comparable to the gain of visually induced self-tilt in erect subjects. Apparently, the contribution of nonvisual cues to gravity was independent of the subject's orientation to gravity itself. It therefore seems that the gain of visually induced self-tilt is smaller because of lacking, rather than conflicting, nonvisual cues. A vector analysis is used to discuss the results in terms of relative sensory weightings.     

The visual cliff: cardiac and behavioral responses on the deep and shallow sides at five and nine months of age

Cardiac and behavioral reactions of 5- and 9-month-old infants placed directly atop the two sides of the visual cliff were studied. Evidence of a developmental shift in infant responses on the deep side of the cliff was obtained in heart rate, which shifted from the deceleration previously obtained with younger subjects, to the acceleration obtained with the 9-month-olds of the present study. Behaviorally, visual attention on the two sides was similar at 5 months, but differed at 9 months, being significantly greater on the deep side. Limb movement showed less of an increase on the deep side than on the shallow at both ages tested. Negative vocalization and positive vocalization recordings failed to show any significant effects. The cardiac data are interpreted as indicating a possible shift from attentiveness to fearfulness on the deep side with age.     

Approximate entropy used to assess sitting postural sway of infants with developmental delay

Infant sitting postural sway provides a window into motor development at an early age. The approximate entropy, a measure of randomness, in the postural sway was used to assess developmental delay, as occurs in cerebral palsy. Parameters used for the calculation of approximate entropy were investigated, and approximate entropy of postural sway in early sitting was found to be lower for infants with developmental delay in the anterior-posterior axis, but not in the medial-lateral axis. Spectral analysis showed higher frequency features in the postural sway of early sitting of infants with typical development, suggesting a faster control mechanism is active in infants with typical development as compared to infants with delayed development, perhaps activated by near-fall events.     

Visually induced reorientation illusions.

It is known that rotation of a furnished room around the roll axis of erect subjects produces an illusion of 360 degrees self-rotation in many subjects. Exposure of erect subjects to stationary tilted visual frames or rooms produces only up to 20 degrees of illusory tilt. But, in studies using static tilted rooms, subjects remained erect and the body axis was not aligned with the room. We have revealed a new class of disorientation illusions that occur in many subjects when placed in a 90 degrees or 180 degrees tilted room containing polarised objects (familiar objects with tops and bottoms). For example, supine subjects looking up at a wall of the room feel upright in an upright room and their arms feel weightless when held out from the body. We call this the levitation illusion. We measured the incidence of 90 degrees or 180 degrees reorientation illusions in erect, supine, recumbent, and inverted subjects in a room tilted 90 degrees or 180 degrees. We report that reorientation illusions depend on the displacement of the visual scene rather than of the body. However, illusions are most likely to occur when the visual and body axes are congruent. When the axes are congruent, illusions are least likely to occur when subjects are prone rather than supine, recumbent, or inverted.     

Two steps forward and one back: Learning to walk affects infants' sitting posture

The transition from sitting to walking is a major motor milestone for the developing postural system. This study examined whether this transition to walking impacts the previously established posture (i.e., sitting). Nine infants were examined monthly from sitting onset until 9 months post-walking. Infants sat on a saddle-shape chair either independently or with their right hand touching a stationary contact surface. Postural sway was measured by sway amplitude, variability, area, and velocity of the center of pressure trajectory. The results showed that for all the postural measures in the no-touch condition, a peak before or at walk onset was observed in all the infants. At the transition age, when peak sway occurred, infants' postural sway measures were significantly greater than at any other age. Further, infants' postural sway was attenuated by touch only at this transition. We suggest that this transient disruption in sitting posture results from a process involving re-calibration of an internal model for the sensorimotor control of posture so as to accommodate the newly emerging bipedal behavior of independent walking.     

The Dynamics of Visual Reweighting in Healthy and Fall-Prone Older Adults

Multisensory reweighting (MSR) is an adaptive process that prioritizes the visual, vestibular, and somatosensory inputs to provide the most reliable information for postural stability when environmental conditions change. This process is thought to degrade with increasing age and to be particularly deficient in fall-prone versus healthy older adults. In the present study, the authors investigate the dynamics of sensory reweighting, which is not well-understood at any age. Postural sway of young, healthy, and fall-prone older adults was measured in response to large changes in the visual motion stimulus amplitude within a trial. Absolute levels of gain, and the rate of adaptive gain change were examined when visual stimulus amplitude changed from high to low and from low to high. Compared with young adults, gains in both older adult groups were higher when the stimulus amplitude was high. Gains in the fall-prone elderly were higher than both other groups when the stimulus amplitude was low. Both older groups demonstrated slowed sensory reweighting over prolonged time periods when the stimulus amplitude was high. The combination of higher vision gains and slower down weighting in older adults suggest deficits that may contribute to postural instability.     

Neuromuscular control of posture in the infant and child: is vision dominant?

This study explored the effects of vision and maturation on the characteristics of neuromuscular responses underlying balance control in both seated and standing children of five age groups (3 1/2-5 months, 8-14 months, 2-3 years, 4-6 years, and 7-10 years). A platform was used to unexpectedly disturb the child's balance in the anterior or posterior direction. Responses of the leg, trunk, and neck muscles were recorded using surface electromyograms. Vision was not required for the activation of these responses in any of the age groups tested. However, comparison of the muscle response latencies of standing children to posterior platform translation in the two visual conditions showed a significant reduction in latency for neck flexors in the 2- to 3-year-olds with vision removed and ann increase in the total number of monosynaptic reflexes. No reduction in latency was found in the older age groups. The hypothesis of a shift from an early long latency visual dominance to a shorter latency proprioceptive one during childhood is discussed. Postural control showed a cephalo-caudal developmental gradient with postural responses appearing first in the neck, then trunk, and finally, legs, as children developed from 3 to 14 months of age. A wide variety of response patterns was seen in the 3- to 5-month-olds, indicating that postural responses are not functional prior to experience with stabilizing the center of mass.     

Neuromuscular Control of Posture in the Infant and Child

This study explored the effects of vision and maturation on the characteristics of neuromuscular responses underlying balance control in both seated and standing children of five age groups (3½–5 months, 8–14 months, 2–3 years, 4–6 years, and 7–10 years). A platform was used to unexpectedly disturb the child’s balance in the anterior or posterior direction. Responses of the leg, trunk, and neck muscles were recorded using surface electromyograms.

Vision was not required for the activation of these responses in any of the age groups tested. However, comparison of muscle response latencies of standing children to posterior platform translation in the two visual conditions showed a significant reduction in latency for neck flexors in the 2- to 3-year-olds with vision removed and an increase in the total number of monosynaptic reflexes. No reduction in latency was found in the older age groups. The hypothesis of a shift from an early long latency visual dominance to a shorter latency proprioceptive one during childhood is discussed.

Postural control showed a cephalo-caudal developmental gradient with postural responses appearing first in the neck, then trunk, and finally, legs, as children developed from 3 to 14 months of age. A wide variety of response patterns was seen in the 3- to 5-month-olds, indicating that postural responses are not functional prior to experience with stabilizing the center of mass.     

Postural orientation: age-related changes in variability and time-to-boundary

The relation between age-specific postural instability and the detection of stability boundaries was examined. Balance control was investigated under different visual conditions (eyes open/closed) and postural orientations (forward/backward lean) while standing on a force platform. Dependent variables included center of pressure variability and the time-to-contact of the center of pressure with the stability boundaries around the feet (i.e., time-to-boundary). While leaning maximally, older individuals (ages 55-69) showed increased center of pressure variability compared to no lean, while younger subjects (ages 24-38) showed a decrease. These significant differences were found only in anterior-posterior direction. No significant age-specific differences were found between eyes open and eyes closed conditions. Time-to-boundary analysis revealed reduced spatio-temporal stability margins in older individuals in both anterior-posterior and medio-lateral directions. Time-to-boundary variability, however, was not significantly different between the groups in both medio-lateral and anterior-posterior direction. These results show the importance of boundary relevant center of pressure measures in the study of postural control, especially concerning the lateral instability often observed in older adults.