Coupling of fingertip somatosensory information to head and body sway

Light touch contact of a fingertip with a stationary surface can provide orientation information that enhances control of upright stance. Slight changes in contact force at the fingertip provide sensory cues about the direction of body sway, allowing attenuation of sway. In the present study, we asked to which extent somatosensory cues are part of the postural control system, that is, which sensory signal supports this coupling? We investigated postural control not only when the contact surface was stationary, but also when it was moving rhythmically (from 0.1 to 0.5 Hz). In doing so, we brought somatosensory cues from the hand into conflict with other parts of the postural control system. Our focus was the temporal relationship between body sway and the contact surface. Postural sway was highly coherent with contact surface motion. Head and body sway assumed the frequency of the moving contact surface at all test frequencies. To account for these results, a simple model was formulated by approximating the postural control system as a second-order linear dynamical system. The influence of the touch stimulus was captured as the difference between the velocity of the contact surface and the velocity of body sway, multiplied by a coupling constant. Comparison of empirical results (relative phase, coherence, and gain) with model predictions supports the hypothesis of coupling between body sway and touch cues through the velocity of the somatosensory stimulus at the fingertip. One subject, who perceived movement of the touch surface, demonstrated weaker coupling than other subjects, suggesting that cognitive mechanisms introduce flexibility into the postural control scheme.     

The influence of dynamic visual cues for postural control in children aged 7–12 years

Young children rely heavily on vision for postural control during the transition to walking. Although by 10 years of age, children have automatic postural responses similar to adults, it is not clear when the integration of sensory inputs becomes fully developed. The purpose of this study was to examine this transition in the sensory integration process in children aged 7–12 years. Healthy children and adults stood on a fixed or sway-referenced support surface while viewing full-field optic flow scenes that moved sinusoidally (0.1 and 0.25 Hz) in an anterior–posterior direction. Center of pressure was recorded, and measures of sway amplitude and phase were calculated at each stimulus frequency. Children and adults had significant postural responses during approximately two-thirds of the trials. In adults, there was a 90% decrease in sway on the fixed surface compared with the sway-referenced surface, but only a 50% decrease in children. The phase between the optic flow stimulus and postural response in children led that of adults by 52° at 0.1 Hz and by 15° at 0.25 Hz. Adults and children aged 7–12 years have similar ability to use dynamic visual cues for postural control. However, 7–12-year-old children do not utilize somatosensory cues to stabilize posture to the same extent as adults when visual and somatosensory cues are conflicting.     

Postural control in children

The purpose of this investigation was to determine whether the coupling between dynamic somatosensory information and body sway is similar in children and adults. Thirty children (4-, 6-, and 8-year-olds) and 10 adults stood upright, with feet parallel, and lightly contacting the fingertip to a rigid metal plate that moved rhythmically at 0.2, 0.5, and 0.8 Hz. Light touch to the moving contact surface induced postural sway in all participants. The somatosensory stimulus produced a broadband frequency response in children, while the adult response was primarily at the driving frequency. Gain, as a function of frequency, was qualitatively the same in children and adults. Phase decreased less in 4-year-olds than other age groups, suggesting a weaker coupling to position information in the sensory stimulus. Postural sway variability was larger in children than adults. These findings suggest that, even as young as age 6, children show well-developed coupling to the sensory stimulus. However, unlike adults, this coupling is not well focused at the frequency specified by the somatosensory signal. Children may be unable to uncouple from sensory information that is less relevant to the task, resulting in a broadband response in their frequency spectrum. Moreover, higher sway variability may not result from the sensory feedback process, but rather from the children's underdeveloped ability to estimate an internal model of body orientation. Electronic Publication     

Development of multisensory reweighting for posture control in children

Reweighting to multisensory inputs adaptively contributes to stable and flexible upright stance control. However, few studies have examined how early a child develops multisensory reweighting ability, or how this ability develops through childhood. The purpose of the study was to characterize a developmental landscape of multisensory reweighting for upright postural control in children 4–10 years of age. Children were presented with simultaneous small-amplitude somatosensory and visual environmental movement at 0.28 and 0.2 Hz, respectively, within five conditions that independently varied the amplitude of the stimuli. The primary measure was body sway amplitude relative to each stimulus: touch gain and vision gain. We found that children can reweight to multisensory inputs from 4 years on. Specifically, intra-modal reweighting was exhibited by children as young as 4 years of age; however, inter-modal reweighting was only observed in the older children. The amount of reweighting increased with age indicating development of a better adaptive ability. Our results rigorously demonstrate the development of simultaneous reweighting to two sensory inputs for postural control in children. The present results provide further evidence that the development of multisensory reweighting contributes to more stable and flexible control of upright stance, which ultimately serves as the foundation for functional behaviors such as locomotion and reaching.     

Dynamics of inter-modality re-weighting during human postural control

Flexible and stable postural control requires adaptation to changing environmental conditions, a process which requires re-weighting of multisensory stimuli. Recent studies, as well as predictions from a computational model, have indicated a reciprocal re-weighting relationship between modalities when a sensory stimulus changes amplitude. As one modality is down-weighted, another is up-weighted to compensate (and vice versa). The purpose of this study was to investigate the dynamics of intra- and inter-modality re-weighting process by examining postural responses to manipulation of proprioception and visual modalities simultaneously. Twenty-two young adults were placed in a visual cave and stood on a variable-pitch platform for thirteen trials of 250 s apiece. The platform was rotated at constant frequency of 0.4 Hz and amplitudes of 0.3 (low) or 1.5 (high) degrees. Platform amplitude was manipulated in two conditions: low-to-high or high-to-low. The visual stimulus was displayed at constant frequency of 0.35 Hz and amplitude of 0.08 degrees. The results showed both fast and slow changes in center of mass (CoM) response to the switch in platform amplitude. On both timescales, CoM response changed in a reciprocal manner relative to platform amplitude. When the platform amplitude increased (low-to-high condition), CoM response decreased relative to the platform and increased relative to the visual stimulus, indicating both intra-modality and inter-modality sensory re-weighting. In the high-to-low condition, however, there was no change in CoM response relative to visual stimulus, indicating that re-weighting may also be dependent on the absolute level of gain. Sway variability at frequencies other than the stimulus frequency also showed a reciprocal relationship with CoM gain relative to platform. Overall, these results indicate that dynamics of multisensory re-weighting is clearly more complicated than the schemes proposed by current adaptive models of human postural control.     

Age-related differences in postural control: effects of the complexity of visual manipulation and sensorimotor contribution to postural performance

Patterns of adaptive changes to the exposure to a sinusoidal visual stimulus can be influenced by stimulus characteristics as well as the integrity of the sensory and motor systems involved in the task. Sensorimotor deficits due to aging might alter postural responses to visual manipulation, especially in more demanding tasks. The purpose of this study was to compare postural control between young and older adults at different levels of complexity and to examine whether possible sensory and/or motor changes account for postural performance differences in older adults. Older and young adults were submitted to the following tests: postural control assessments, i.e., body sway during upright stance and induced by movement of a visual scene (moving room paradigm); sensory assessments, i.e., visual (acuity and contrast sensitivity) and somatosensory (tactile foot sensitivity and detection of passive ankle motion); and motor assessments, i.e., isometric ankle torque and muscular activity latency after stance perturbation. Older adults had worse sensory and motor performance, larger body sway amplitude during stance and stronger coupling between body sway and moving room motion than younger adults. Multiple linear regression analyses indicated that the threshold for the detection of passive ankle motion contributed the most to variances in body sway and this contribution was more striking when visual information was manipulated in a more unpredictable way. The present study suggests that less accurate information about body position is more detrimental to controlling body position, mainly for older adults in more demanding tasks.     

Auditory biofeedback substitutes for loss of sensory information in maintaining stance

The importance of sensory feedback for postural control in stance is evident from the balance improvements occurring when sensory information from the vestibular, somatosensory, and visual systems is available. However, the extent to which also audio-biofeedback (ABF) information can improve balance has not been determined. It is also unknown why additional artificial sensory feedback is more effective for some subjects than others and in some environmental contexts than others. The aim of this study was to determine the relative effectiveness of an ABF system to reduce postural sway in stance in healthy control subjects and in subjects with bilateral vestibular loss, under conditions of reduced vestibular, visual, and somatosensory inputs. This ABF system used a threshold region and non-linear scaling parameters customized for each individual, to provide subjects with pitch and volume coding of their body sway. ABF had the largest effect on reducing the body sway of the subjects with bilateral vestibular loss when the environment provided limited visual and somatosensory information; it had the smallest effect on reducing the sway of subjects with bilateral vestibular loss, when the environment provided full somatosensory information. The extent that all subjects substituted ABF information for their loss of sensory information was related to the extent that each subject was visually dependent or somatosensory-dependent for their postural control. Comparison of postural sway under a variety of sensory conditions suggests that patients with profound bilateral loss of vestibular function show larger than normal information redundancy among the remaining senses and ABF of trunk sway. The results support the hypothesis that the nervous system uses augmented sensory information differently depending both on the environment and on individual proclivities to rely on vestibular, somatosensory or visual information to control sway.     

Modeling postural instability with Galvanic vestibular stimulation

In this study the effect of a pseudorandom binaural bipolar Galvanic stimulus generated by a sum of nonharmonically related sine waves on postural control was functionally assessed using computerized dynamic posturography (CDP), and the results compared to vestibulopathic patient populations and astronauts exposed to microgravity. The standardized CDP test battery comprised six sensory organization tests (SOTs) that combined three visual conditions (eyes open, eyes closed, and sway-referenced vision) with two proprioceptive conditions (fixed and sway-referenced support surfaces). Subjects (12) performed 18 randomized trials (three trials of each of the six SOTs) as a baseline, repeated the 18 trials with Galvanic vestibular stimulation (GVS), and then performed a post-GVS baseline. A 10 min rest period was inserted between each test battery. Anterioposterior postural sway increased significantly and was in the abnormal range (fifth percentile) during GVS for SOTs where visual input was compromised (sway-referenced surround) or absent. Postural stability returned to baseline when GVS was removed. An analysis of sensory input scores (somatosensory, visual, and vestibular) demonstrated the specificity of GVS in distorting vestibular input to postural control. The SOT scores observed in astronauts on landing day did not differ significantly to that generated by GVS in our normal subjects. GVS also induced a similar pattern of instability on CDP as profound bilateral vestibular loss, although not as severe. The results suggest that unpredictably varying GVS quantitatively and qualitatively models postural instability of vestibular origin.     

Attentional demands associated with the use of a light fingertip touch for postural control during quiet standing

The purpose of the present experiment was to investigate whether and how using a light fingertip touch for postural control during quiet standing requires additional attentional demands. Nine young healthy university students were asked to respond as rapidly as possible to an unpredictable auditory stimulus while maintaining stable seated and upright postures in three sensory conditions: vision, no-vision and no-vision/touch. Touch condition involved a gentle light touch with the right index finger on a nearby surface at waist height. Center of foot pressure (CoP) displacements were recorded using a force platform. Reaction times (RTs) values were used as an index of the attentional demand necessary for calibrating the postural system. Results showed decreased CoP displacements in both the vision and no-vision/touch conditions relative to the no-vision condition. More interestingly, a longer RT in the no-vision/touch than in the vision and no-vision conditions was observed. The present findings suggest that the ability to use a light fingertip touch as a source of sensory information to improve postural control during quiet standing is attention demanding.     

Postural strategies associated with somatosensory and vestibular loss

Summary This study examines the roles of somatosensory and vestibular information in the coordination of postural responses. The role of somatosensory information was examined by comparing postural responses of healthy control subjects prior to and following somatosensory loss due to hypoxic anesthesia of the feet and ankles. The role of vestibular information was evaluated by comparing the postural responses of control subjects and patients with bilateral vestibular loss. Postural responses were quantified by measuring 1) spatial and temporal characteristics of leg and trunk EMG activation; 2) ankle, knee, and hip joint kinematics, and 3) surface forces in response to anterior and posterior surface translations under different visual and surface conditions. Results showed that neither vestibular nor somatosensory loss resulted in delayed or disorganized postural responses. However, both types of sensory deficits altered the type of postural response selected under a given set of conditions. Somatosensory loss resulted in an increased hip strategy for postural correction, similar to the movement strategy used by control subjects while standing across a shortened surface. Vestibular loss resulted in a normal ankle strategy but lack of a hip strategy, even when required for the task of maintaining equilibrium on a shortened surface. Neither somatosensory nor vestibular loss resulted in difficulty in utilizing remaining sensory information for orientation during quiet stance. These results support the hypothesis that cutaneous and joint somatosensory information from the feet and ankles may play an important role in assuring that the form of postural movements are appropriate for the current biomechanical constraints of the surface and/or foot. The results also suggest that vestibular information is necessary in controlling equilibrium in a task requiring use of the hip strategy. Thus, both somatosensory and vestibular sensory information play important roles in the selection of postural movement strategies appropriate for their environmental contexts.     

Multisensory control of human upright stance

The interaction of different orientation senses contributing to posture control is not well understood. We therefore performed experiments in which we measured the postural responses of normal subjects and vestibular loss patients during perturbation of their stance. Subjects stood on a motion platform with their eyes closed and auditory cues masked. The perturbing stimuli consisted of either platform tilts or external torque produced by force-controlled pull of the subjects' body on a stationary platform. Furthermore, we presented trials in which these two stimuli were applied when the platform was body-sway referenced (i.e., coupled 1:1 to body position, by which ankle joint proprioceptive feedback is essentially removed). We analyzed subjects' postural responses, i.e., the excursions of their center of mass (COM) and center of pressure (COP), using a systems analysis approach. We found gain and phase of the responses to vary as a function of stimulus frequency and in relation to the absence versus presence of vestibular and proprioceptive cues. In addition, gain depended on stimulus amplitude, reflecting a non-linearity in the control. The experimental results were compared to simulation results obtained from an 'inverted pendulum' model of posture control. In the model, sensor fusion mechanisms yield internal estimates of the external stimuli, i.e., of the external torque (pull), the platform tilt and gravity. These estimates are derived from three sensor systems: ankle proprioceptors, vestibular sensors and plantar pressure sensors (somatosensory graviceptors). They are fed as global set point signals into a local control loop of the ankle joints, which is based on proprioceptive negative feedback. This local loop stabilizes the body-on-foot support, while the set point signals upgrade the loop into a body-in-space control. Amplitude non-linearity was implemented in the model in the form of central threshold mechanisms. In model simulations that combined sensor fusion and thresholds, an automatic context-specific sensory re-weighting across stimulus conditions occurred. Model parameters were identified using an optimization procedure. Results suggested that in the sway-referenced condition normal subjects altered their postural strategy by strongly weighting feedback from plantar somatosensory force sensors. Taking this strategy change into account, the model's simulation results well paralleled all experimental results across all conditions tested.     

Individuals with post-stroke hemiparesis are able to use additional sensory information to reduce postural sway

The present study aimed to investigate whether stroke survivals are able to use the additional somatosensory information provided by the light touch to reduce their postural sway during the upright stance. Eight individuals, naturally right-handed pre-stroke, and eight healthy age-matched adults stood as quiet as possible on a force plate during 35 s. Participants performed two trials for each visual condition (eyes open and closed) and somatosensory condition (with and without the right or left index fingertip touching an instrumented rigid and fixed bar). When participants touched the bar, they were asked to apply less than 1 N of vertical force. The postural sway was assessed by the center of pressure (COP) displacement area, mean amplitude and velocity. In addition, the mean and standard deviation of the force vertically applied on the bar during the trials with touch were assessed. The averaged values of COP area, amplitude and velocity were greater for stroke individuals compared to healthy adults during all visual and somatosensory conditions. For both groups, the values of all variables increased when participants stood with eyes closed and reduced when they touched the bar regardless of the side of the touch. Overall, the results suggested that, as healthy individuals, persons with post-stroke hemiparesis are able to use the additional somatosensory information provided by the light touch to reduce the postural sway.     

Multisensory information for postural control: sway-referencing gain shapes center of pressure variability and temporal dynamics

The authors investigated the multisensory control of posture by altering sensory information across the visual and somatosensory systems. The support surface and visual surround were sway-referenced to anterior/posterior center of mass sway and the gain between postural sway and degree of sway referencing was manipulated (gain settings were 0.2, 1.0, and 1.8). These alterations in the sensory environment lead to observed changes in the temporal structure of the center of pressure (COP) trajectories. COP path length increased across gain settings while COP coefficient of variation decreased. The COP became increasingly more deterministic across more challenging sensory organization test (SOT) conditions and with increasing gain, and more nonstationary across more challenging SOT conditions and when the support surface was sway-referenced using a 1.8 gain setting. These findings indicate that changes in the responsiveness of the support surface and/or visual surround within each of the sway-referenced SOT conditions had functional consequences for the control of posture as evidenced by the variations in postural sway dynamics.     

Controlling human upright posture: velocity information is more accurate than position or acceleration

The problem of how the nervous system fuses sensory information from multiple modalities for upright stance control remains largely unsolved. It is well established that the visual, vestibular, and somatosensory modalities provide position and rate (e.g., velocity, acceleration) information for estimation of body dynamics. However, it is unknown whether any particular property dominates when multisensory information is fused. Our recent stochastic analysis of postural sway during quiet stance suggested that sensory input provides more accurate information about the body's velocity than its position or acceleration. Here we tested this prediction by degrading major sources of velocity information through removal/attenuation of sensory information from vision and proprioception. Experimental measures of postural sway were compared with model predictions to determine whether sway behavior was indicative of a deficit in velocity information rather than position or acceleration information. Subjects stood with eyes closed on a support surface that was 1) fixed, 2) foam, or 3) sway-referenced. Six measures characterizing the stochastic structure of postural sway behaved in a manner consistent with model predictions of degraded velocity information. Results were inconsistent with the effect of degrading only position or acceleration information. These findings support the hypothesis that velocity information is the most accurate form of sensory information used to stabilize posture during quiet stance. Our results are consistent with the assumption that changes in sway behavior resulting from commonly used experimental manipulations (e.g., foam, sway-referencing, eyes closed) are primarily attributed to loss of accurate velocity information.     

Postural dynamics and habituation to seasickness

The computerized dynamic posturography (CDP) test examines the response pattern to simultaneous, multimodal sensory stimulation. The purpose of this prospective, controlled study was to investigate whether postural dynamics evaluated by CDP are related to seasickness severity and the process of habituation to sea conditions. Subjects included 74 naval personnel assigned to service aboard ship and 29 controls designated for shore-based positions. Study participants performed a baseline CDP test, and subsequent follow-up examinations 6 and 12 months after completion of their training. On those occasions they also completed a seasickness severity questionnaire. Longitudinal changes in postural parameters were examined, as well as a possible correlation between baseline CDP results and final seasickness severity scores. The results indicated longitudinal habituation to seasickness. Reduced scores were found for sensory organization sub-tests 3 and 5 in the first follow-up examination, reflecting increased weighting of visual and somatosensory input in the maintenance of balance. Scores in the second follow-up examination were above baseline values, indicating increased reliance on vestibular cues. These significant bimodal changes were found only in study subjects having the highest degree of habituation to seasickness. A significant decrease in motor response strength was found in parallel with increased habituation to seasickness. Baseline CDP results and postural control dynamics were not correlated with subjects’ final seasickness severity score. These results suggest a potential role for CDP in monitoring the process of habituation to unusual motion conditions.     

Postural control during quiet standing following cervical muscular fatigue: effects of changes in sensory inputs

The purpose of the present experiment was to investigate the effects of cervical muscular fatigue on postural control during quiet standing under different conditions of reliability and/or availability of somatosensory inputs from the plantar soles and the ankles and visual information. To this aim, 14 young healthy adults were asked to sway as little as possible in three sensory conditions (No vision, No vision-Foam support and Vision) executed in two conditions of No fatigue and Fatigue of the scapula elevator muscles. Centre of foot pressure (CoP) displacements were recorded using a force platform. Results showed that (1) the cervical muscular fatigue yielded increased CoP displacements in the absence of vision, (2) this effect was more accentuated when somatosensation was degraded by standing on a foam surface and (3) the availability of vision allowed the individuals to suppress this destabilising effect. On the whole, these findings not only stress the importance of intact cervical neuromuscular function on postural control during quiet standing, but also suggest a reweigthing of sensory cues in balance control following cervical muscular fatigue by increasing the reliance on the somatosensory inputs from the plantar soles and the ankles and visual information.     

Dental occlusion and postural control in adults

We studied the influence of a dental occlusion perturbation on postural control. The tests were performed in three dental occlusion conditions: (Rest Position: no dental contact, Maximal Intercuspal Occlusion: maximal dental contact, and Thwarted Laterality Occlusion: simulation of a dental malocclusion) and four postural conditions: static (stable platform) and dynamic (unstable platform), with eyes open and eyes closed. A decay of postural control was noted between the Rest Position and Thwarted Laterality Occlusion conditions with regard to average speed and power indexes in dynamic conditions and with eyes closed. However, the head position and stabilization were not different from those in the other experimental conditions, which means that the same functional goal was reached with an increase in the total energetic cost. This work shows that dental occlusion differently affects postural control, depending on the static or dynamic conditions. Indeed, dental occlusion impaired postural control only in dynamic postural conditions and in absence of visual cues. The sensory information linked to the dental occlusion comes into effect only during difficult postural tasks and its importance grows as the other sensory cues become scarce.     

Role of somatosensory and vestibular cues in attenuating visually induced human postural sway

The purpose of this study was to determine the contribution of visual, vestibular, and somatosensory cues to the maintenance of stance in humans. Postural sway was induced by full-field, sinusoidal visual surround rotations about an axis at the level of the ankle joints. The influences of vestibular and somatosensory cues were characterized by comparing postural sway in normal and bilateral vestibular absent subjects in conditions that provided either accurate or inaccurate somatosensory orientation information. In normal subjects, the amplitude of visually induced sway reached a saturation level as stimulus amplitude increased. The saturation amplitude decreased with increasing stimulus frequency. No saturation phenomena were observed in subjects with vestibular loss, implying that vestibular cues were responsible for the saturation phenomenon. For visually induced sways below the saturation level, the stimulus-response curves for both normal subjects and subjects experiencing vestibular loss were nearly identical, implying (1) that normal subjects were not using vestibular information to attenuate their visually induced sway, possibly because sway was below a vestibular-related threshold level, and (2) that subjects with vestibular loss did not utilize visual cues to a greater extent than normal subjects; that is, a fundamental change in visual system gain was not used to compensate for a vestibular deficit. An unexpected finding was that the amplitude of body sway induced by visual surround motion could be almost 3 times greater than the amplitude of the visual stimulus in normal subjects and subjects with vestibular loss. This occurred in conditions where somatosensory cues were inaccurate and at low stimulus amplitudes. A control system model of visually induced postural sway was developed to explain this finding. For both subject groups, the amplitude of visually induced sway was smaller by a factor of about 4 in tests where somatosensory cues provided accurate versus inaccurate orientation information. This implied (1) that the subjects experiencing vestibular loss did not utilize somatosensory cues to a greater extent than normal subjects; that is, changes in somatosensory system gain were not used to compensate for a vestibular deficit, and (2) that the threshold for the use of vestibular cues in normal subjects was apparently lower in test conditions where somatosensory cues were providing accurate orientation information.     

Nonlinear postural control in response to visual translation

Recent models of human postural control have focused on the nonlinear properties inherent to fusing sensory information from multiple modalities. In general, these models are underconstrained, requiring additional experimental data to clarify the properties of such nonlinearities. Here we report an experiment suggesting that new or multiple mechanisms may be needed to capture the integration of vision into the postural control scheme. Subjects were presented with visual displays whose motion consisted of two components: a constant-amplitude, 0.2 Hz oscillation, and constant-velocity translation from left to right at velocities between 0 cm/s and 4 cm/s. Postural sway variability increased systematically with translation velocity, but remained below that observed in the eyes-closed condition, indicating that the postural control system is able to use visual information to stabilize sway even at translation velocities as high as 4 cm/s. Gain initially increased as translation velocity increased from 0 cm/s to 1 cm/s and then decreased. The changes in gain and variability provided a clear indication of nonlinearity in the postural response across conditions, which were interpreted in terms of sensory reweighting. The fact that gain did not decrease at low translation velocities suggests that the postural control system is able to decompose relative visual motion into environmental motion and self-motion. The eventual decrease in gain suggests that nonlinearities in sensory noise levels (state-dependent noise) may also contribute to the sensory reweighting involved in postural control. These results provide important constraints and suggest that multiple mechanisms may be required to model the nonlinearities involved in sensory fusion for upright stance control.