Aging and the mechanisms underlying head and postural control during voluntary motion.

Key Words: Balance, Head control, Posture, Sensory integration.

The quality of sensory information that is necessary for balance and postural stability depends to a great extent on head stabilization as the body moves. Some investigators have proposed that a "top-down" or "head-first" control scheme is used to ensure that the head remains stable, with respect to the direction of looking, during body movement.(1-4) Head stability allows gaze (the direction of looking) to be properly oriented.(1-4) This orientation is supposedly accomplished by modifying head position in anticipation of displacements in the body's center of force (COF)(*) so that the angular orientation of the head in space remains relatively constant. Anticipatory control of the angular displacement of the head is referred to as a head-stabilization-in-space (HSS) strategy (Fig. 1).(6) This strategy differs from a response that fixes the head to the trunk, because the HSS allows adjustments of head position that are independent of trunk motion (Fig. 1).(6,7)

Stabilizing the head in advance of body motion is thought to improve the interpretation of vestibular inputs for balance,(6,8) particularly when visual and somatosensory inputs are distorted or incongruent.(6) Sensory inputs that yield conflicting perceptions of motion are considered to be incongruent. For example, visual cues are incongruent with vestibular inputs when vision conveys the sense of motion in the environment but vestibular information indicates that the body is stationary with respect to gravity. Asymptomatic elderly persons have demonstrated the ability to use multiple sensory inputs for balance as long as two of three primary modalities visual, vestibular, or somatosensory inputs--are available.(9,10) Changes in the sensorimotor system with aging have been well documented,(11-13) but these changes have not been studied with respect to head stabilization in older persons. Age-related changes in the vestibular ocular reflex(14) (VOR), for example, could distort visual input during activities of daily living such as walking. A deficient VOR impairs the ability to fix eye position while the head is moving.(15) One way to partially compensate for a deficient VOR is to stabilize the head in away that nullifies the effect of body motion. The HSS, therefore, would provide one compensatory strategy that elderly persons might use to improve gaze.

Whether the HSS strategy is used by elderly people to stabilize gaze during movement or whether the natural changes in sensory processing with age alter the head stabilization strategy is not known. Hirasaki et al(16) studied the influence of various locomotor activities on compensatory head pitch motions (counteracting vertical translations of the body during gait) in subjects over 60 years of age, but the influence of sensory inputs on head control was not addressed in the experimental design. Although some authors have addressed the control of head stabilization during support-surface perturbations.(8,17-20); during voluntary motions such as walking, hopping, or running(1,2,6,21-23); and during rotations of the entire body,(24,25) the populations studied were primarily younger than 60 years of age. Balance in elderly persons has been assessed using altered sensory environments,(9,26-29) platform perturbations,(26,27) and voluntary motion to test the limits of stability,(30,31) but there have not been systematic investigations addressing the integration of sensory inputs for head control in aging populations.

The purpose of this article is to present a theoretical basis for understanding the influence of aging on head control during voluntary motion. In addition, a discussion of some preliminary research findings that demonstrate how elderly individuals might utilize a head control strategy to improve gaze and the quality of vestibular inputs for balance will be provided. The discussion of theory is organized into four content areas: 1) frames of reference for balance and head control, 2) sensory influences on each frame of reference, 3) development of head control strategies, and 4) presentation of a conceptual model of head control mechanisms. A presentation of the results of some preliminary studies that demonstrate head stabilization strategies in older persons follows the discussion of theory.

Theoretical Mechanisms Underlying Head Control During Voluntary Motion

Frames of Reference for Balance and Head Control A frame of reference for balance is a standard against which a change in posture is measured.(32,33) There are three frames of reference that are relevant to the discussion of head and postural control.(32-34) An egocentric reference frame provides spatial coordinates for limb and body-segment positions (eg, head position relative to the trunk), whereas an exocentric reference gives information about body position with respect to the environment (eg, visual localization of an object that is extrinsic to the subject). A geocentric reference system maintains posture with respect to gravity (vertical orientation). Berthoz(32) and Paillard(33) suggested that the relative importance of each frame of reference was organized in a hierarchy, with the egocentric and exocentric frames of reference derived from a geocentric reference system.

Frames of reference for head and postural control, in theory, have several common characteristics.(32,33) Each frame of reference is produced by the transformation of sensory input to spatial perception. In addition, each reference system contributes to the development of an overall body schema or template for balance, and the frames of reference enable the prediction of displacements of the COF.

Transformation of sensory input. Information from visual, vestibular, and proprioceptive systems are transformed in each frame of reference to contribute to aspects of postural control that are not sensor-specific. For example, there is no single dedicated sensor in the nervous system that measures the "margin of postural stability" during stance.(35) This variable can only be derived from an interpretative process within the central nervous system (CNS) that utilizes sensory inputs to estimate the configuration of the support surface, the magnitude and sequence of postural muscle activity, and the location of the center of gravity.(35) The "sense" of the limit of postural stability, therefore, is a perception based on one or more frames of reference for balance.

Contribute to a body schema. Head and Holmes defined body schema as "a combined standard against which all subsequent changes of posture are measured."(36) They emphasized that the body schema is a template for postural control that influences spatial orientation of the body "before a change of posture enters consciousness." From a theoretical perspective, the body schema can be viewed as the collective influence of the egocentric, exocentric, and geocentric frames of reference for balance.

Enable the prediction of movement. A primary goal of postural regulation is to stabilize the head with respect to the vertical.(32,33) To provide effective control of head position during movement, the geocentric frame of reference enables anticipation or prediction of COF displacements that are induced by voluntary, motion.(32,34) The geocentric frame of reference is thought to use somatosensory, proprioceptive, and vestibular inputs for "feed-forward" control of head stabilization. In the context of a "top-down" or "head-first" control model,(4,6) feed-forward means that corrections of head position occur in advance of a voluntary change in body position. A feed-forward mechanism is a preprogrammed (predetermined) response that appears to be formed through experience with self-initiated goal-directed activity.(34) Sensory input in a feed-forward mode is used primarily for "knowledge of response" to make appropriate adjustments in subsequent anticipatory postural actions.(37) This interative process is thought to develop various frames of reference that make up the template (body schema) to control head and trunk orientation for balance. (35,37,38)

Sensory Influence on the Frames of Reference for Balance and Head Control

The literature reviewed in this section highlights three issues. First, a geocentric frame of reference is essential for generating anticipatory control of head position during voluntary motion. Distortions or absence of sensory input results in an improvement of feed-forward stabilization of the head as long as the geocentric reference is intact.(6) Second, the frames of reference for balance are not based on the input from a single sensory modality. Each frame of reference is derived from multiple sensory inputs.(33,35,39-43) Third, there are interactions among the frames of reference that contribute to the internal representation of a body schema and the overall perception of head, trunk, and limb orientation.(32,33,35,44) The contribution of various sensory modalities to each frame of reference for head stability and postural control will be reviewed.

Vestibular influence on the geocentric frame of reference. The labyrinth provides two types of information about head kinematics: 1) orientation of static head posture with respect to gravity and 2) detection of head acceleration.(45-53) The vestibular inputs that sense static head posture provide the backdrop for anticipatory or "feed-forward" control of head position(4,6) by continuously monitoring the orientation of the head.(45,46) The otolith organs provide an invariant reference for head position with respect to earth-vertical.(47) An example of this static gravitational reference can be illustrated by the ocular counter-rolling reflex. When the head is tilted to the side, the eyes counter-rotate to nullify the effects of head motion(51,53) and maintain vertical orientation of the visual scene (Fig. 2). Vestibular input, therefore, is used for repositioning of the eyes based on changes in head orientation (a more detailed review of visual-vestibular interactions is beyond the scope of this article, but the reader should refer to the article by Herdman in this special series and to a review by Cohen and Henn(54)).

Vestibular inputs also influence trunk and limb stability when head position changes. The functional linkage between head orientation and lower-extremity muscle activity was demonstrated by Zangemeister et al.(55) They used a backward head tilt to enhance the influence of the otolith end organs during gait for five subjects without impairments (mean age=97 years). Zangemeister et al(55) found that tibialis anterior muscle discharge markedly increased during the entire walking cycle and also showed a phasic burst of activity at mid-stance. This pattern of tibialis anterior muscle activity was thought to represent a feed-forward postural adjustment mediated by the otolith organs in anticipation of the COF displacements (beyond the base of support) that normally occur during gait.

When vestibular input is absent, there is a loss of postural stabilization that normally occurs prior to self-initiated voluntary motion. The loss of anticipatory postural control following vestibular dysfunction is manifest by the loss of feed-forward control of the head.(56-61) Deficits in the anticipatory control of head position occur in persons without vestibular dysfunction who are exposed to microgravity and in patients with bilateral vestibular dysfunction. Astronauts returning to Earth from orbit in space experience difficulty coordinating head and trunk motion during gait, and as a result they experience temporary postural instability.(22) Reschke et al(22) have suggested that the absence of gravity results in recalibration of the otolith gravity receptors so that the ambiguities between the sense of linear motion during gait and the sense of gravity contribute to a loss of feed-forward head control. Bronstein(56) studied six patients with vestibular loss (32-78 years of age) and six subjects without vestibular impairment (18-62 years of age) who were seated in a chair and rotated in random directions while the subjects attempted to fixate on a visual target. The subjects without vestibular impairment were able to anticipate changes in the direction of chair rotation and corrected head position in advance of the changes in trunk (chair) position. In contrast, subjects with bilateral vestibular deficits did not show this feed-forward adjustment in head position.(56) Other researchers have shown that subjects with bilateral vestibular deficits have larger head displacement amplitudes, angular velocities, or gaze velocities (motion of the eyes with respect to the head) in the dark during hopping or running(57-59) and walking in place(60,61) compared with subjects without vestibular impairment.

Somatosensory influence on geocentric frame of reference.

Because bilateral vestibular dysfunction results in a loss of anticipatory head control, it is reasonable to conclude that vestibular inputs that monitor the resting position of the head appear to be necessary to establish feed-forward control of head position. Vestibular inputs, however, may not be sufficient to completely form or elaborate the geocentric reference because other sensory inputs are known to lead to modification of head position with respect to the vertical. Somatosensory (cutaneous, joint, and pressure receptors) as well as muscle proprioception from spindle afferents, for example, can shape the geocentric reference for balance and head stabilization.(3,35,39-41,62)

Evidence that somatosensory inputs to the CNS influence the geocentric frame of reference for head stability was provided in separate investigations by Pozzo et al,(3) Young and Standish,(39) and Jeka and colleagues.(40,41) Pozzo et al(3) observed that during a self-initiated jumping motion, there was an unbroken trajectory of head rotation in the sagittal plane in spite of the impact of foot-floor contact. They suggested that physical contact between the foot and the floor provided the capacity to predict a perturbation of gaze and provide anticipator), neck muscle contraction to correct impending head displacement.(3) Light touch from the fingertip may also provide somatosensory input to the CNS that contributes to head stabilization.(39-41) Young and Standish(39) showed that visually induced postural sway was attenuated in seven of nine subjects without vestibular impairment when light tactile pressure (insufficient to stabilize posture) was applied to the shoulder. Jeka et al(41) found that sighted individuals with eyes closed had a decrease in head and COF displacement when only light fingertip contact (<2.0 N) was placed on a cane during tandem stance. Postural sway in subjects with congenital blindness also improved with touch cues gained by fingertip contact, but head stability did not improve.(41) These results suggested that persons with congenital blindness were unable to integrate somatosensory information to control head displacement.(41) As noted, considerable sensory processing must occur to transform tactile information to orientation information. Head stability, therefore, appears to depend on a geocentric frame of reference that integrates vestibular inputs with somatosensory inputs from both upper- and lower-extremity load-bearing surfaces to stabilize the head with respect to the vertical.

Mittelstaedt(63) has argued that the geocentric reference is strongly influenced by somatic gravity receptors originating from the viscera within the trunk. There is preliminary evidence suggesting that somatic gravity, receptors exist in monkeys(64) and in humans,(65) but further study is needed to reproduce these findings and to determine the influence of these receptors on the control of head stabilization.

Influence of vision on the geocentric frame of reference.

Visual input (retinal information) does not appear to be needed for head stabilization.(1,3,4,6) The alteration of visual inputs by darkness or stroboscopic illumination actually improved head stabilization in space during hopping and running,(1,3) locomotion,(6) and stance within a tilting visual enclosure.(43) Collectively, these results suggest that in the absence of normal visual input, a feed-forward mode of head stabilization may control head position in a precise way so that the remaining sensory inputs (ie, vestibular and somatosensory) can provide optimal orientation information.

Influence of gaze and muscle proprioception on egocentric and exocentric frames of reference. Gaze is the intended direction of looking and occurs as a result of eye muscle activation. Factors that determine gaze are the position of the eyes in the head and the position of the head in three-dimensional space. Gaze contributes to both the exocentric and egocentric frames of reference. The "egocentric" component of gaze exists because the muscles that control eye movements provide proprioceptive feedback that is used to control the spatial orientation of the head and trunk.(66,67) Gaze is also "exocentric," because there is evidence that spindle afferent information from muscles surrounding the eye help localize visual targets in the environment.(68) The influence that gaze has on the egocentric and exocentric frames of reference for balance, therefore, is thought to be related to proprioception provided by the ocular muscles (the term "proprioception," as used here, refers specifically to muscle spindle afferent information).

Alteration of the egocentric and exocentric frames of reference can be studied by applying vibration to a muscle or tendon.(44,62,66-71) Vibration alters the perception of limb localization(44,66,67,69,70) (distorting the egocentric frame of reference) as well as the localization of objects viewed in the environment (distorting the exocentric frame of reference).(68,71) A classic example of altering the egocentric frame of reference was provided by Goodwin et al,(69) who showed that vibration of the Achilles tendon in restrained standing subjects can create the illusion of forward body sway. If subjects are not restrained, stimulation of the Achilles tendon results in a corrective body sway backward, because the CNS acts to correct the perceived body tilt.(66,67,70) Several investigators(66,67,70) have reported that vibration of the extraocular inferior rectus muscles or the sternocleidomastoid muscles of freely standing subjects with eyes closed induces the same corrective postural response that is observed with soleus muscle vibration. A proprioceptive linkage between the head, trunk, and lower extremities that controls head and body orientation was proposed to explain the analogous postural effects of muscle vibration at these different sites.(66) For each vibrated muscle, corrective body sway was presumed to be related to a perceived change in the egocentric frame of reference.(66,67,70)

Alterations in the exocentric frame of reference have been studied with subjects in a sitting position or by restraining standing subjects from swaying during muscle vibration. In these conditions, subjects not only experience an illusion of sway, as described earlier, but also a perception that fixed visual targets are moving.(66,68) Distortion of the exocentric frame of reference was demonstrated by Roll et al.(68) They studied 10 subjects without vestibular impairment during a task involving pointing toward a fixed visual target.(68) The subjects were seated in the dark and were instructed to point toward the lighted target once the light was extinguished. Low-amplitude vibration of the eye or neck muscles changed the direction of pointing to correspond to the direction of head motion that would have stretched the vibrated muscle (ie, pointing drifted upward during vibration of sternocleidomastoid muscles or the extra-ocular inferior rectus muscles). Similar findings with other neck muscles were reported by Biguer et al.(71) Roll et al(68) and Biguer et al(71) presumed, therefore, that spindle afferent input to the CNS from the vibrated muscle altered the localization of visual targets because of a change in the exocentric frame of reference.

In summary, feed-forward control of head position occurs against the backdrop of a constant geocentric reference. Vestibular information signaling static head tilt with respect to gravity is necessary to enable anticipatory stabilization of the head, but somatosensory and proprioceptive inputs are also needed to refine the head stabilization response and the geocentric reference for balance. Minimizing head motion when sensory information is absent or distorted is desirable, because head stabilization can reduce the ambiguity of sensory inputs for balance. This "protective mechanism" might account for the improvement in head Stabilization during the distortion or absence of visual input. Proprioceptive inputs from Ocular and postural muscles appear to have an influence on geocentric, egocentric, and exocentric frames of reference for balance. There appears to be a "functional synergy" between eye, limb, and trunk muscles that influences the control of head and trunk orientation.

Development of Anticipatory Head Control Strategies

Hayes and Riach(37) proposed that sensory inputs serve three purposes in a feed-forward control system for balance: 1) identification of the initial stance conditions (ie, position, orientation, and motion of the body), 2) provision of immediate information about the feed-forward response once it has been initiated (ie, knowledge of response if balance was maintained), and 3) provision of feedback that is used over the long term to improve the effectiveness of subsequent feed-forward responses. The visual and vestibular end organs are located in the head. The quality and "usability" of these sensory inputs for identifying initial conditions depends, therefore, to a great extent on the strategy used to control head position prior to voluntary motion.

Assaiante and Amblard(6) reported that children 3 to 6 years of age used an HSS strategy while walking on flat ground (Fig. 1). This strategy involves the correction of head position in advance of the rhythmic body oscillations produced during gait. When an equilibrium task became more difficult for these children (ie, walking on a narrow beam), there was an increase in head-trunk stiffness that resembled a head-stabilization-on-trunk (HST) strategy (Fig. 1). The HST strategy reduces the need for anticipatory correction of head position because the head and trunk tend to move as a single unit. Adults, by comparison, showed a preference for the HSS strategy, particularly during difficult equilibrium tasks.(6)

The inability of children under 6 years of age to adopt the HSS strategy during difficult equilibrium tasks suggests that the neural signals that specify head position with respect to the base of support are not fully integrated by the CNS at this age. There is evidence showing that infants just beginning to walk independently attempt to use sensory feedback to develop head-trunk control.(72) Ledebt et al(72) reported a marked improvement in head-trunk control during the first 10 to 15 weeks after the onset of independent walking. The delay between the initiation of walking and the improvement in head-trunk coordination was attributed to the development of neural processing to integrate sensory inputs for equilibrium during ambulation.(72) Feed-forward postural adjustments may develop in parallel with the maturation of sensory feedback processes.(37) Whether the degradation of sensory processing attributed to aging, in turn, degrades the mechanisms that produce anticipatory head stabilization during voluntary motion is not known.

Conceptual Model of Head Control During Voluntary Motion

Head stabilization as the body moves is partly an expression of righting reflexes, the passive elastic and viscous properties of muscle and connective tissue surrounding head and neck body segments, and "higher-order" sensory mechanisms.(73) The body schema and frames of reference for head stability are higher-order sensory mechanisms that must play a dominant role in the control of head position during voluntary motion, because the ability to anticipate the location of the center of gravity and correct head position in advance of a change in body posture requires the integration of multiple sensory inputs. Head control, therefore, cannot be viewed simply as a vestibular reflex or a passive tissue response.

The higher-order mechanisms that link sensory inputs to the control of head stabilization have not been delineated. Schor et al(74) speculated that feedback provided by muscle proprioceptors and somatosensory information contributes to the voluntary and reflex responses that underlie head control. Light-touch cues, for example, could increase the efficiency of head stabilization through the cervicocollic reflex, because this reflex relies on peripheral somatosensory inputs to monitor the position of the head with respect to the body.(74) In parallel with this reflex "loop," a neuronal network facilitating the interaction between ankle somatosensory inputs with information from proprioceptors along the vertical axis of the body--including information from neck, trunk, and eye muscles--could also influence head displacement prior to the initiation of voluntary motion.(66,67,75-77)

We are proposing a preliminary conceptual model that uses a template for head stabilization based on the body schema (Fig. 3). The body schema for head and trunk orientation is influenced by vestibular and other sensory inputs. The amplitude and direction of anticipatory stabilization of the head will depend on the initial conditions established by sensory input to the body schema. Angular orientation of the head in space in this model is corrected at a subconscious level after a change in one or more frames of reference, but in advance of the conscious initiation of voluntary motion. Head stabilization in turn reinforces the body schema in a feedback loop by minimizing an immediate change in eye position (stabilizing retinal input), the position of the vestibular end organs, and the position of the neck (stabilizing neck somatosensory and proprioception inputs). Head control, in this model, is influenced by sensory inputs through the frames of reference for balance, rather than directly by individual sensory modalities. Once the head is stabilized, trunk and extremity postural control follows. This action creates sensory feedback and "knowledge of response" that can be used to modify the body schema for subsequent action.

The geocentric frame of reference in this model is at the top of a hierarchy with respect to the other frames of reference.(32,33) The geocentric frame of reference is necessary, but not sufficient for feed-forward control of the head. Other frames of reference (ie, egocentric or exocentric) are needed to fully form the response for anticipatory head stabilization. The invariant gravitational reference provided by the geocentric system provides a protective mechanism that ensures angular stability of the head during difficult balance tasks.(6) Task difficulty is determined by mechanical factors (eg, stance on a narrow surface,(6,19) stance on a compliant support surface,(9) single-leg stance(29)) or by the availability or quality of sensory information (ie, balance while walking in the dark or with stroboscopic illumination).(6) The HSS strategy (Fig. 1) is a feed-forward control strategy that, theoretically, will be useful during difficult balance tasks because the precise control of angular head displacement optimizes the quality of available sensory inputs that will contribute to proper orientation of the body (Fig. 3).

Demonstration of Head Stabilization Strategies in Older Persons

Experimental Paradigm and Research Questions

We have completed several experiments(43,78,79) that begin to examine the ability of elderly people to produce head stabilization strategies that might protect gaze and stabilize sensory inputs for balance. The experimental paradigm that we utilized involved balance tasks that have different levels of difficulty (Figs. 4 and 5). Subjects stood on a movable force platform and faced a visual enclosure (described in more detail later). The level of difficulty was controlled by changing the coupling--referred to as the "gain"--between body sway and simultaneous tilt of the platform or visual surround. For example, any displacement of the COF at a gain of +2.0 will create a tilt of the visual surround (away from the subject) or a tilt of the platform (toes down) that will be four times larger than a tilt at a gain of +0.5 (Figs. 4 and 5). Changing the polarity of the gain to negative reverses the direction of the surround or platform motion (ie, as the COF moves forward, the surround is tilted toward the subject or the platform is rotated toes up). Balance in the negative gain conditions was more challenging than balance in the positive gain conditions, because the environment in a negative gain condition moved completely opposite the direction of body sway. Greater frequency or amplitude of corrective balance responses in the negative gain conditions compared with the positive gain conditions (described in the "Findings" section) confirmed the relative difficulty of the negative gain conditions. It was possible, therefore, to evaluate head stabilization using a spectrum of task difficulty by altering the stability of the support surface (platform tilt) or by distorting visual input (surround tilt).

We studied two research questions: 1) Do elderly people use the HSS strategy to control head position during more difficult balance tasks? and 2) Do the head stabilization strategies used by elderly people differ, descriptively, from those strategies implemented by younger persons? With regard to the first research question, many elderly people without vestibular symptoms (ie, those without a history of falling, frequent dizziness, or vertigo) have difficulty interpreting sensory inputs that provide conflicting information about spatial orientation.(9,10,26) For this reason, it seemed reasonable to propose that older persons would need to enhance their ability to use sensory inputs that contribute to each frame of reference for balance, particularly in conditions with sensory incongruence. We hypothesized that elderly persons would rely on the HSS strategy to optimize the quality of sensory input for balance.

In formulating the second research question, we considered previous findings that postural stability decreases with age.(80-82) To compensate for age-related deterioration in postural stability, elderly individuals without vestibular symptoms may develop greater control of head position compared with younger individuals. This strategy would allow elderly to efficiently use sensory inputs that contribute to each frame of reference discussed earlier. We hypothesized, therefore, that elderly persons without vestibular symptoms would have greater head stabilization compared with younger persons.

The methods used to study these research questions are outlined in the Appendix, and the experimental conditions are summarized in Table 1.

Outcome Measures

Head stability was analyzed by comparing the peak-to-peak head motion with the peak-to-peak displacement of the COF in the sagittal plane for each trial. The ratio of head motion to COF displacement was referred to as the head mobility score (HMS). An HMS was calculated for sagittal translation of the head (head-x HMS) and for rotation of the head in the sagittal plane (pitch HMS). The HMS provided an index for detecting relative changes in head-body coupling. Larger HMS values indicated that the head was moving greater distances with respect to the COF, as compared with a lower HMS. The relative extent of head stabilization in space between experimental conditions, therefore, could be compared using the HMS ratios. A pitch HMS of 0.5, for example, means that the peak-to-peak pitch rotation of the head per unit of COF displacement was half as much as a pitch HMS of 1.0. The head is relatively more stable in space with respect to body motion, therefore, with a lower HMS.

Data analysis. Each subject served as his or her own control. Baseline values for head-x and pitch HMS were evaluated using paired t tests for each age group (pretest versus posttest). For the experimental conditions, trials with positive gains were paired with the corresponding trial utilizing a negative gain of the same absolute value. Paired t tests were done for each dependent variable (head-x and pitch HMS) in each sensory condition (surround motion [SM], eyes open-platform motion [EO-PM], and eyes closed-platform motion [EC-PM]). The experimentwise error rate was adjusted using a Bonferroni correction for multiple comparisons (P<.025).

Findings

Baseline measurements. Baseline HMS measurements in stance on a fixed platform and fixed visual surround with eyes open (EO-FPS) and eyes closed (EC-FPS) did not differ from pretest to posttest measurement for elderly subjects or for younger subjects (Fig. 6). The increase in peak-to-peak COF displacement at the posttest measurement compared with the pretest measurement (Fig. 6) was offset by a parallel increase in head displacement. The net result was that the head-x and pitch HMS ratios remained relatively constant from pretest to posttest measurement.

Head stabilization response to sway-driven tilt of visual surround. There were decreases in head-x and pitch HMS (Tab. 2 and Fig. 7) for younger subjects in the negative, more challenging gain conditions compared with the positive gain conditions. Elderly subjects also showed a decrease in head-x HMS (Tab. 2), and there was a nonsignificant finding that pitch HMS decreased in negative gain compared with positive gain conditions (t=-1.92, df=23, P=.067; Tab. 2 and Fig. 8), although the probability value for the decrease in pitch HMS was close to being significant.

Head stabilization response to sway-driven tilt of the platform: eyes open. In young subjects, there was no change in the head-x HMS for positive versus negative gain during EO-PM (Tab. 2). The pitch HMS for young subjects, however, increased during negative gains compared with positive gains (Tab. 2 and Fig. 9). In contrast, elderly subjects showed a reduction in the head-x HMS and a nonsignificant reduction of the pitch HMS (Tab. 2 and Fig. 9) in negative gains compared with positive gains (t=-2.31, df=23, P=.03), although the probability value for the reduction of pitch HMS was close to being significant. The frequency and amplitude of corrective adjustments in the COE were greater for the negative gain conditions (see "Elderly Subjects," Fig. 9) compared with the positive gain conditions. Head pitch remained stable in spite of the COF fluctuations.

Head stabilization response to sway-driven tilt of the platform: eyes closed. Young subjects showed no change in head-x HMS, whereas elderly subjects had a decrease in this variable (Tab. 2 and Fig. 10). There were small increases in the pitch HMS for younger subjects in negative versus positive gains, but there was no change in the pitch HMS for elderly subjects (Tab. 2). The frequency of corrective adjustments in the COF for the negative gain conditions (for both young and elderly subjects; Fig. 10) was greater compared with the frequency for the positive gain conditions. Head pitch remained stable for all subjects in spite of these frequent COF adjustments.

Discussion

There are no specific sensors in the body that signal the sequence of limb motion, the position of the center of gravity, or the dimensions of a support surface.(35,62) The control or spatial perception of these variables requires a body schema--an internal representation of the head and body orientation--that serves as a template for balance and equilibrium. The body schema can be viewed as the collective expression of egocentric, exocentric, and geocentric frames of reference (Fig. 3). Anticipatory head stabilization that accompanies voluntary motion occurs because these frames of reference for balance enable the prediction or anticipation of a change in the position of the COF. Stabilization of the head in a feed-forward manner, in turn, optimizes the quality of sensory inputs that are used for equilibrium.(3,4,6,22)

Minimizing head motion during more difficult balance tasks is desirable because head stabilization can reduce the ambiguity of sensory inputs that contribute to the body schema. In our preliminary studies, we demonstrated that elderly subjects without vestibular symptoms restrained head motion to a greater extent in conditions where mechanical compliance of the force platform or distortion of visual inputs was most disruptive to equilibrium (eg, in the negative gain conditions; Figs. 8-10). The HSS strategy in older persons was apparent from the tight control of head pitch when the balance tasks were most challenging. This finding means that older persons could use a HSS strategy to control head position during active balance tasks as an effective way to stabilize the head in a feed-forward manner during a wide range of COF displacements (Figs. 8-10). Confirmation of these preliminary results awaits further testing, but the observations in this study appear to demonstrate the theory that elderly persons might use an HSS strategy to stabilize the head.

Age-related differences in processing proprioceptive inputs have been reported by Quoniam et al,(70) who showed that vibration-induced postural sway was slower and had less amplitude for 26 elderly subjects (60-88 years of age) than for 9 younger subjects (20-44 years of age). This finding implies that elderly persons underestimate the dysequilibrium that is signaled by the proprioceptive systems. The reduction of corrective sway amplitude and velocity for the elder subjects might also suggest that elderly persons process incongruent sensory inputs less efficiently than do younger persons, and therefore have a greater need to constrain body tilt during balance activities. The results from our preliminary study support this idea. Specifically, during conditions that distorted proprioceptive inputs from the lower extremities (EO-PM and EC-PM), elderly subjects showed either an attenuation of the pitch HMS (EO-PM) or no change in the pitch HMS from positive to negative gain conditions. The mean pitch HMS for the elderly subjects never increased during the transition from positive to negative gains (Tab. 2). In contrast, younger subjects increased the pitch HMS, and this increase occurred most markedly in EO-PM (Tab. 2 and Fig 9). The implication of the preliminary findings is that elderly persons without vestibular symptoms may actually constrain head motion to a greater extent than younger persons in an attempt to optimize the quality of visual and vestibular inputs for balance. Additional research is necessary to further evaluate this theory.

The adjustments in head position prior to initiation of voluntary movement are not likely to influence body stabilization because of the relatively low mass of the head.(7) By contrast, anticipatory postural adjustments in the limbs (ie, activation of the thigh muscles to stabilize the knee prior to rapid ankle plantar flexion while standing) appear to stabilize the body in preparation for movement initiation.(83-90) A complete discussion of anticipatory postural adjustments in the limbs is beyond the scope of this article. Feed-forward control of head position and limb position are important for successful balance behavior, but for different reasons. Head stabilization may optimize the quality of sensory inputs used by the CNS to activate postural muscles for balance (Fig. 3), whereas the preparatory muscle activation in the limbs ensures postural stability during task initiation.(7,83-90) The "functional synergies" between eye, limb, and trunk muscles that were described earlier may provide a fundamental mechanism that could enhance the coordination of head stabilization with the preparatory limb stabilization that occurs prior to initiation of voluntary movement.

The postural control mechanisms underlying self-initiated voluntary motion(1,3,6) may be different from those controlling balance during a reaction to external perturbation.(8,17-20) Shupert et al,(19) for example, found that head motion did not appear to be coordinated with ankle or hip motion when subjects reacted to perturbations of stance on a flat surface or a transverse beam. These authors suggested that changes in the neck angle were passively propagated up the body following lower-extremity reaction to support surface displacement (ie, primarily viscoelastic rather than active control of head position). This reactive response to perturbation was different from the anticipatory head stabilization that has been reported for self-initiated voluntary motion.(1,3,6) More work is needed to clarify how aging influences the mechanisms controlling head stability during "reactive" postural adjustments compared with goal-directed voluntary movements.

Clinical Implications

Balance during voluntary motion requires that patients gain precise control of head motion. In persons with neurologic dysfunction, it is possible that disruption of sensory integration may alter anticipatory head stabilization and lead to balance dysfunction during self-initiated motion. Many types of treatment have been advocated for patients with deficits in the ability to integrate sensory information for balance.(29,91) These treatments often involve practicing standing while the therapist alters the availability or congruence of sensory inputs. Patients who rely on "support surface" cues for orientation, for example, are asked to practice balance and walking on compliant surfaces such as foam or moving surfaces. The goal is to train patients to become proficient with balance in progressively more difficult conditions by altering or distorting available sensory information (a more detailed review of the treatment procedures is provided by Shumway-Cook and McCollum(91)). These procedures, however, do not specifically address the control of head motion as a distinct feature in the treatment protocol.

Some interventions have been described that focus on the control of the head as a means of facilitating overall postural control.(92) The "Alexander Technique," for example, involves positioning the head prior to voluntary motion as a way of integrating the flow of head and body action (reviewed by Jones ). Jones(92) found that the coordination of head-body motion observed during activities such as walking, stair climbing, or raising from a chair was altered when the position of the head was modified prior to the beginning of the task. He suggested that changes in head posture would facilitate more efficient movement patterns.(92) There has been little recent attention to this procedure in the literature, but some of the concepts advanced by Alexander (eg, that head control will influence overall postural stability) are supported by the "top-down" or "head-first" scheme of postural organization described in our review.

Although balance is often disrupted following a lesion of the CNS, loss of head control has not been specifically addressed in many patient populations that require physical therapy. It is known that certain CNS deficits alter anticipatory postural adjustment. For example, when subjects with stroke perform a rapid voluntary sway, the number of response defaults (the number of times that postural muscles are not recruited) is greater than for subjects who are not disabled.(93) When a postural response is initiated, "anticipatory" activation of the paretic limb occurs closer in time to the intended movement. Patients with hemiplegia appear to be unable to fully integrate anticipatory, feed-forward components of balance to execute a voluntary motion.(94) Furthermore, prior knowledge of the task constraints--usually in a nonchoice reaction-time paradigm--does not improve the onset or timing of feed-forward postural adjustments(84,93,95) or change the sequence of postural muscle activation following stroke.(96) Therapy aimed at head control during voluntary motion may improve anticipatory postural responses in the lower limbs of patients after strokes, but this idea warrants further study.

Conclusions

Voluntary, self-initiated movement involves feed-forward, anticipatory control of head position. The mechanism of head stabilization seems to rely primarily on a geocentric frame of reference, but can be refined by egocentric or exocentric frames of reference. Increasing the difficulty of balance tasks might increase the dominance of an HSS strategy in older persons. The HSS strategy will theoretically optimize the use of sensory inputs for balance. There is some support for addressing head stabilization within the context of a "top-down" or "head-first" control scheme, and alternative treatments for balance dysfunction might be developed using this theoretical framework. The development of treatment strategies that address head control during voluntary motion seems to be justified from the theoretical constructs and preliminary findings reported here. The implementation of new treatments based on the "head-first" model will require additional study.

Acknowledgments

We sincerely appreciate the help of Jennifer Suarez and Danielle R Di Fabio for their assistance with manuscript preparation.

* Center of force is the location of the vertical ground reaction force vector measured by a force platform and is equal and opposite to a weighted average of all of the downward forces acting on the force plate.(5)

Table 1.
Pretest/Posttest and Block Randomization of Tester-Selected
Gain Across Sensory Conditions

                                                         No.
                                                         of
                   Sensory Condition[a]       Gain      Trials

Pretest            EO-FPS                       0         3
                   EC-FPS                       0         3
Gain-block
randomization
  A                SM, EO-PM, EC-PM            +0.5       3
                                               -0.5       3
  B                SM, EO-PM, EC-PM            +1.0       3
                                               -1.0       3

  C                SM, EO-PM, EC-PM            +1.5       3
                                               -1.5       3

  D                SM, EO-PM, EC-PM            +2.0       3
                                               -2.0       3
Posttest           EO-FPS                       0         3
                   EC-FPS                       0         3

[a] Eyes open (EO-FPS) and eyes closed (EC-FPS) with a fixed platform and visual surround; gain blocks A-D systematically randomized and presented during sensory conditions with surround motion (SM), platform motion with eyes open (EO-PM) and eyes closed (EC-PM).

Table 2.
Head-x and Pitch Head Mobility Scores for Each Age Group and
Gain Polarity During Visual Surround Motion (SM) and With Eyes
Open (EO-PM) and Eyes Closed (EC-PM) During Stance on a Movable
Platform

                              Under 50 Years of Age
                              Positive Gain     Negative Gain
Condition         Motion      X        SD       X         SD

SM                Head-x      1.54     0.42     1.37a     0.33
                  Pitch       1.80     0.96     1.44a     0.85
EO-PM             Head-x      1.05     0.31     1.10      0.37
                  Pitch       0.99     0.58     1.48c     0.79
EC-PM             Head-x      1.27     0.29     1.24      0.19
                  Pitch       0.64     0.56     0.91c     0.54
No. of trials                60                60


                              Over 65 Years of Age
                              Positive Gain     Negative Gain
Condition         Motion      X        SD       X         SD

SM                Head-x      1.51     0.28     1.31a     0.29
                  Pitch       1.41     0.63     1.14b     0.53
EO-PM             Head-x      1.27     0.39     1.07b     0.25
                  Pitch       1.40     1.29     0.85b     0.27
EC-PM             Head-x      1.40     0.30     1.21a     0.23
                  Pitch       0.67     0.35     0.76      0.29
No. of trials                24                24

X bar over X

a Significantly lower compared with positive gain; P <.025.

b Trend for lower head mobility score compared with positive gain; .025<P[less than or equal to].07.

c Significantly greater compared with positive gain; P <.025.

References

1 Pozzo T, Berthoz A, Lefort L. Head stabilization during various locomotor tasks in humans, I: normal subjects. Exp Brain Res. 1990;82: 97-106.

2 Bloomberg JJ, Reschke MF, Huebner WP, Peters BT. The effects of target distance on eye and head movement during locomotion. Ann NY Acad Sci. 1992;656:699-707.

3 Pozzo T, Berthoz A, Lefort L. Head kinematics during various motor tasks in humans. Prog Brain Res. 1989;80:377-383.

4 Berthoz A, Pozzo T. intermittent head stabilization during postural and locomotory tasks in humans. In: Amblard B, Berthoz A, Clarac F, eds. Posture and Gait: Development, Adaptation, and Modulation. Amsterdam, the Netherlands: Elsevier Science Publishers BV; 1988:189-198.

5 Winter DA. Biomechanics and Motor Control of Human Movement. 2nd ed. New York, NY: John Wiley & Sons Inc; 1990:93-95.

6 Assaiante C, Amblard B. Ontogenesis of head stabilization in space during locomotion in children: influence of visual cues. Exp Brain Res. 1993;93:499-515.

7 Gurfinkel VS, Lipshits MI, Lestienne FG. Anticipatory neck muscle activity associated with rapid arm movements. Neurosci Lett. 1988;94: 104-108.

8 Allum JHJ, Keshner EA, Honegger F, Pfaltz CR. Organization of leg-trunk-head equilibrium movements in normals and patients with peripheral vestibular deficits. Prog Brain Res. 1988;76:277-290.

9 Whipple R, Wolfson L, Derby C, et al. Altered sensory function and balance in older persons. J Gerontol. 1993;48:71-76.

10 Woollacott MH. Age-related changes in posture and movement. J Gerontol. 1993;48:56-60.

11 Brocklehurst JC, Robertson D, James-Groom P. Clinical correlates of sway in old age sensory modalities. Age Ageing. 1982;11:1-10.

12 Lord SR, Clark RD, Webster IW. Postural stability and associated physiological factors in a population of aged persons. J Gerontol Med Sci. 1991;46:M69-M76.

13 Lord SR, Webster IW. Visual field dependence in elderly fallers and non-fallers. Int J Aging Hum Dev. 1990;31:267-277.

14 Paige GD. Senescence of human visual-vestibular interactions, 1: vestibulo-ocular reflex and adaptive plasticity with aging. J Vestib Res. 1992;2:133-151.

15 King OS, Seidman SH, Leigh RJ. Control of head stability and gaze during locomotion in normal subjects and patients with deficient vestibular function. In: Berthoz A, Graf W, Vidal PP, eds. The Head-Neck Sensory Motor System. New York, NY: Oxford University Press Inc; 1992:568-570.

16 Hirasaki E, Kubo T, Nozawa S, et al. Analysis of head and body movements of elderly people during locomotion. Acta Otolaryngol (Stockh). 1993;501:25-30.

17 Takahashi M. Head stability and gaze during vertical whole-body oscillations. Ann Otol Rhinol Laryngol. 1990;99:883-888.

18 Murata T, Kitahara M. Acceleration registrography of head movement during alternating inclination of the support platform. Acta Otolaryngol (Stockh). 1994;510:33-37.

19 Shupert CL, Black FO, Horak FB, Nashner LM. Coordination of the head and body in response to support surface translations in normals and patients with bilaterally reduced vestibular function. In: Amblard B, Berthoz A, Clarac F, eds. Posture and Gait: Development, Adaptation, and Modulation. Amsterdam, the Netherlands: Elsevier Science Publishers BV; 1988:281-289.

20 Nashner LM, Shupert CL, Horak FB. Head-trunk movement coordination in the standing posture. Prog Brain Res. 1988;76:243-251.

21 Grossman GE, Leigh RJ, Abel LA, et al. Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res. 1988;70:470-476.

22 Reschke MF, Bloomberg JJ, Harm DL, Paloski WH. Space flight and neurovestibular adaptation. J Clin Pharmacol. 1994;34:609-617.

23 Dichgans J, Diener HC. The contribution of vestibulo-spinal mechanisms to the maintenance of human upright posture. Acta Otolaryngol (Stockh). 1989;107:338-345.

24 Keshner EA, Peterson BW. Motor control strategies underlying head stabilization and voluntary head movements in humans and cats. Prog Brain Res. 1988;76:329-339.

25 Guitton D, Kearney RE, Wereley N, Peterson BW. Visual, vestibular, and voluntary contributions to human head stabilization. Exp Brain Res. 1986;64:59-69.

26 Woollacott MH, Shumway-Cook A, Nashner LM. Aging and posture control: changes in sensory organization and muscular coordination. Intl J Aging Hum Dev. 1986;23:97-119.

27 Wolfson L, Whipple R, Derby CA, et al. Gender differences in the balance of healthy elderly as demonstrated by dynamic posturography. J Gerontol Med Sci. 1994;49:M160-M167.

28 Simoneau GG, Leibowitz HW, Ulbrecht JS, et al. The effects of visual factors and head orientation on postural steadiness in women 55 to 70 years of age. J Gerontol Med Sci. 1992;47:M151-M158.

29 Hu M-H, Woollacott MH. Multisensory training of standing balance in older adults, I: postural stability and one-leg stance. J Gerontol Med Sci. 1994;49:M52-M61.

30 Blaszczyk JW, Hansen PD, Lowe DL. Postural sway and perception of the upright stance stability borders. Perception. 1993;22:1333-1341.

31 Schieppati M, Hugon M, Grasso M, et al. The limits of equilibrium in young and elderly normal subjects and in Parkinsonians. Electroencephalogr Clin Neurophysiol. 1994;93:286-298.

32 Berthoz A. Reference frames for the perception and control of movement. In: Paillard J, ed. Brain and Space. New York, NY: Oxford University Press Inc; 1991:81-111.

33 Paillard J. Motor and representational framing of space. In: Paillard J, ed. Brain and Space. New York, NY: Oxford University Press Inc; 1991:163-182.

34 Massion J. Movement, posture, and equilibrium: interaction and coordination. Prog Neurobiol. 1992;38:35-56.

35 Gurfinkel VS, Ivanenko YuP, Levik YuS, Babakova IA. Kinesthetic reference for human orthograde posture. Neuroscience. 1995;68:229-243.

36 Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain. 1911-1912;34:102-254.

37 Hayes KC, Riach CL. Preparatory postural adjustments and postural sway in young children. In: Woollacott MH, Shumway-Cook A, eds. Development of Posture and Gait Across the Life Span. Columbia, SC: University of South Carolina Press; 1989:97-127.

38 Lestienne FG, Gurfinkel VS. Posture as an organizational structure based on a dual process: a formal basis to interpret changes of posture in weightlessness. In: Pompeiano O, Allum JHJ, eds. Prog Brain Res. 1988;76(special issue):307-313.

39 Young LR, Standish G. Influence of tactile cues on visually induced postural reactions. In: Berthoz A, Graf W, Vidal PP, eds. The Head-Neck Sensory Motor System. New York, NY: Oxford University Press Inc; 1992:555-559.

40 Jeka JJ, Lackner JR. Fingertip contact influences human postural control. Exp Brain Res. 1994;100:495-502.

41 Jeka JJ, Easton RD, Bentzen BL, Lackner JR. Haptic cues for orientation and postural control in sighted and blind individuals. Perception and Psychophysics. 1996;58:409-423.

42 Berthoz A. The role of gaze in the compensation of vestibular dysfunction: the gaze substitution hypothesis. In: Pompeiano O, Allum JHJ, eds. Prog Brain Res. 1988;76(special issue):411-420.

43 Di Fabio RP, Emasithi A. Effects of aging on adaptation of head control during exposure to sway-driven visual field displacement. Phys Ther. 1996;76:S22. Abstract.

44 Lackner JR. Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain. 1988;111:281-297.

45 Fernandez C, Goldberg J. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey, I: response to static tilts and to long-duration centrifugal force. J Neurophysiol. 1976:39:970-984.

46 Loe PR, Tompko DL, Werner G. The neural signal of angular head position in primary afferent vestibular nerve axons. J Physiol (Lond). 1973:230:29-50.

47 Mayne R. A systems concept of the vestibular organs. In: Kornhuber HH, ed. Handbook of Sensory Physiology Volume 6, Part 2: Vestibular System. New York, NY: Springer Publishing Co Inc; 1974:493-580.

48 Fernandez C, Goldberg J. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey, III: response dynamics. J Neurophysiol. 1976:39:996-1008.

49 Barlow JS. Inertial navigation as a basis for animal navigation. J Theor Biol. 1964;6:76-117.

50 Paige GD, Tomko DL. Eye movement responses to linear head motion in the squirrel monkey, I: basic characteristics. J Neurophysiol. 1991;65:1170-1182.

51 Collewijn H, Van Der Steen J, Ferman L, Jansen TC. Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings. Exp Brain Res. 1985;59:185-196.

52 Lichtenberg BK, Young LR, Arrott AP. Human ocular counterrolling induced by varying linear accelerations. Exp Brain Res. 1982;48: 127-136.

53 Gresty MA, Bronstein AM. Visually controlled spatial stabilisation of the human head: compensation for the eye's limited ability to roll. Neurosci Lett. 1992;140:63-66.

54 Cohen B, Henn V, eds. Representation of Three-Dimensional Space in the Vestibular, Oculomotor, and Visual Systems: A Symposium of the Barany Society. New York, NY: The New York Academy of Sciences; 1988.

55 Zangemeister WH, Bulgheroni MV, Pedotti A. Differential influence of vertical head posture during walking. In: Berthoz A, Graf W, Vidal PP, eds. The Head-Neck Sensory Motor System. New York, NY: Oxford University Press Inc; 1992:560-567.

56 Bronstein AM. Evidence for a vestibular input contribution to dynamic head stabilization in man. Acta Otolaryngol (Stockh). 1988;105: 1-6.

57 Pozzo T, Berthoz A, Lefort L, Vitte E. Head stabilization during various locomotor tasks in humans, II: patients with bilateral peripheral vestibular deficits. Exp Brain Res. 1991;85:208-217.

58 Pozzo T, Berthoz A, Vitte E, Lefort L. Head stabilization during locomotion. Acta Otolaryngol (Stockh). 1991;481:322-327.

59 Takahashi M, Hoshikawa H, Tsujita N, Akiyama I. Effect of labyrinthine dysfunction upon head oscillation and gaze during stepping and running. Acta Otolaryngol (Stockh). 1988;106:348-353.

60 Taguchi K, Hirabayashi C, Kikukawa M. Clinical significance of head movement while stepping. Acta Otolaryngol Suppl (Stockh). 1984; 406:125-128.

61 Grossman GE, Leigh RJ. Instability of gaze during locomotion in patients with deficient vestibular function. Ann Neurol. 1990;27:528-532.

62 Gurfinkel VS, Levik YuS, Popov KE, et al. Body scheme in the control of postural activity. In: Stance and Motion: Third Soviet-French Roundtable Meeting on Neurobiology 1986, Moscow and Leningrad. New York, NY: Plenum Press; 1988:185-193.

63 Mittelstaedt H. Evidence of somatic graviception from new and classical investigations. Acta Otolaryngol Suppl (Stockh). 1995;520:186-187.

64 Ito T, Sanada Y. Location of receptors for righting reflexes acting upon the body in primates. Jpn J Physiol. 1965;15:235-242.

65 Mittelstaedt H. Somatic versus vestibular gravity reception in man. Ann NY Acad Sci. 1992;656:124-139.

66 Roll JP, Roll R. From eye to foot: a proprioceptive chain involved in postural control. In: Amblard B, Berthoz A, Clarac F, eds. Posture and Gait: Development, Adaptation, and Modulation. Amsterdam, the Netherlands: Elsevier Science Publishers BV; 1988:155-164.

67 Roll JP, Vedel JP, Roll R. Eye, head, and skeletal muscle spindle feedback in the elaboration of body references. Prog Brain Res. 1989; 80:113-123.

68 Roll R, Velay JL, Roll JP. Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities. Exp Brain Res. 1991;85:423-431.

69 Goodwin GM, McCloskey DI, Matthews PBC. The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralyzing joint afferents. Brain. 1972;95:705-748.

70 Quoniam C, Hay L, Roll J-P, Harlay F. Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration. J Gerontol Biol Sci. 1995;50:B155-B165.

71 Biguer B, Donaldson IML, Hein A, Jeannerod M. Neck muscle vibration modifies the representation of visual motion and direction in man. Brain. 1988;111:1405-1424.

72 Ledebt A, Bril B, Wiener-Vacher S. Trunk and head stabilization during the first months of independent walking. Neuroreport. 1995;6: 1737-1740.

73 Peterson BW, Richmond FJ. Control of Head Movement. New York, NY: Oxford University Press Inc; 1988.

74 Schor RH, Kearney RE, Dieringer N. Reflex stabilization of the head. In: Peterson BW, Richmond FJ, eds. Control of Head Movement. Oxford, United Kingdom: Oxford University Press; 1988:141-166.

75 Horstmann GA, Dietz V. A basic control mechanism: the stabilization of the centre of gravity. Electroencephalogr Clin Neurophysiol. 1990; 76:165-176.

76 Dietz V, Horstmann G, Berger W. Involvement of different receptors in the regulation of human posture. Neurosci Lett. 1988;94:82-87.

77 Dietz V, Horstmann GA, Trippel M, Gollhofer A. Human postural reflexes and gravity: an underwater simulation. Neurosci Lett. 1989;106: 350-355.

78 Emasithi A, Di Fabio RP. Head position and orientation after exposure to altered sensory environments in different age groups. Phys Ther. 1996;76:S22. Abstract.

79 Di Fabio RP, Emasithi A. Aging and the influence of visual inputs on head stabilization during stance on a rotating surface. Phys Ther. 1996;76:S21. Abstract.

80 Sheldon JH. The effect of age on the control of sway. Geront Clin. 1963;5:129-138.

81 Overstall PW, Exton-Smith AN, Imms FJ, Johnson AL. Falls in the elderly related to postural imbalance. BMJ. 1977;1:261-264.

82 Thyssen HH, Brynskov J, Jansen EC, et al. Normal ranges in reproducibility for quantitative Romberg's test. Acta Neurol Scand. 1982;66:100-104.

83 Badke MB, Di Fabio RP. Effects of postural bias during support surface displacements and rapid arm movements. Phys Ther. 1985;65: 1490-1495.

84 Diener HC, Bacher M, Guschlbauer B, Dichgans J. The coordination of posture and voluntary movement in patients with hemiparesis. J Neurol. 1993;240:161-167.

85 Massion J. Postural changes accompanying voluntary movement: normal and pathological aspects. Human Neurobiology. 1984;2:261-267.

86 Belenkii VY, Gurfinkel VS, Pal'tsev YI. Elements of control of voluntary movements. Biofizika. 1967;12:135-141.

87 Bouisset S, Zattara M. A sequence of postural movement precedes voluntary movement. Neurosci Lett. 1981;22:263-270.

88 Brown JE, Frank JS. Influence of event anticipation on postural actions accompanying voluntary movement. Exp Brain Res. 1987;67: 645-650.

89 Cordo PJ, Nashner LM. Properties of postural adjustments associated with rapid arm movements. J Neurophysiol. 1982;47:287-302.

90 Friedli WG, Hallett M, Simon SR. Postural adjustments associated with rapid voluntary arm movements, I: electromyographic data. J Neurol Neurosurg Psychiatry. 1984;47:611-622.

91 Shumway-Cook A, McCollum G. Assessment and treatment of balance deficits. In: Montgomery PC, Connolly BH, eds. Motor Control and Physical Therapy: Theoretical Framework and Practical Implications. Hixson, Tenn: Chattanooga Group Inc; 1991:123-138.

92 Jones FP. Method for changing stereotyped response patterns by the inhibition of postural sets. Psychol Rev. 1965;72:411-425.

93 Di Fabio RP, Badke MB. Reliability of postural response as a function of muscular synergisms: effect of supraspinal lesions. Human Movement Science. 1989;8:447-464.

94 Di Fabio RP. Adaptation of postural stability following stroke. Topics in Stroke Rehabilitation. 1997;3:62-75.

95 Pal'tsev YI, El'ner AM. Preparatory and compensatory period during voluntary movement in patients with involvement of the brain of different localization. Biofizika. 1967;12:142-147.

96 Horak FB, Esselman P, Anderson ME, Lynch MK. The effects of movement velocity, mass displaced, and task certainty on associated postural adjustments made by normal and hemiplegic individuals. Journal of Neurosurgery and Psychiatry. 1984;47:1020-1028.

RP Di Fabio is Professor and Director of Doctoral Graduate Studies, Program in Physical Therapy, Department of Physical Medicine and Rehabilitation, University of Minnesota, UMHC Box 388, 420 Delaware St SE, Minneapolis, MN 55455 (USA) ([e-mail]). Address all correspondence to Dr Di Fabio.

A Emasithi, PT, is a doctoral student in the Department of Physical Medicine and Rehabilitation and the Department of Kinesiology, University of Minnesota.