Interaction between Visual and Proprioceptive Analyzers in Vertical Posture Control

The CNS can precisely assess the spatial position of the human body only by simultaneously processing and integrating the visual, proprioceptive, and vestibular inputs. Postural stability data make it possible to estimate changes taking place in the function of analyzers involved in the maintenance of the upright posture. The vertical posture stability was assessed in healthy children and children with spastic diplegic cerebral palsy from their postural responses to the presentation of single optokinetic or somatosensory stimuli. The visual analyzer was found to play a significant role in maintaining the upright position under natural gravity conditions in healthy children. A single exposure of the proprioceptive system to variable forces directed with the gravity of the earth (vertical) decreased the contribution of the visual analyzer. Healthy children maintained the upright position relying on the direction of movement of the optokinetic stimuli, which, however, produced no effect on the maintenance of posture in the patients. A hypothesis is proposed that prenatal or early postnatal CNS lesions decrease the contribution of phylogenetically newer brain structures to the regulation of upright posture.     

Effect of ageing and vision on limb load asymmetry during quiet stance

Although the identification and characterization of limb load asymmetries during quiet standing has not received much research attention, they may greatly extend our understanding of the upright stance stability control. It seems that the limb load asymmetry factor may serve as a veridical measure of postural stability and thus it can be used for early diagnostic of the age-related decline in balance control. The effects of ageing and of vision on limb load asymmetry (LLA) during quiet stance were studied in 43 healthy subjects (22 elderly, mean age 72.3+/-4.0 yr, and 21 young, mean age 23.9+/-4.8 yr). Postural sway and body weight distribution were recorded while the subject was standing on two adjacent force platforms during two 120 s trials: one trial was performed with the eyes open (EO), while the other trial was with the eyes closed (EC). The results indicate that LLA was greater in the old adults when compared with the young control subjects. The LLA values were correlated with the postural sway magnitudes especially in the anteroposterior direction. Eyes closure which destabilized posture resulted in a significant increase of body weight distribution asymmetry in the elderly but not in the young persons. The limb load difference between EO and EC conditions showed a significantly greater effect of vision on LLA in the elderly compared to the young subjects. The observed differences in the LLA may be attributed to the decline of postural stability control in the elderly. Ageing results in the progressive decline of postural control and usually the nervous system requires more time to complete a balance recovery action. To compensate for such a deficiency, different compensatory strategies are developed. One of them, as evidenced in our study, is preparatory limb unload strategy (a stance asymmetry strategy) which could significantly shorten reaction time in balance recovery.     

Influence of passive tactile contact of arms on the maintenance of upright posture in humans

The influence of light passive contact of the forearm with a pliable external object (flexible plate) on the maintenance of upright posture was studied in healthy subjects in several conditions, with the eyes closed and on immersion in a virtual visual environment (VVE). The visual environment was either stable or unstable as a result of a synphase (SP) or antiphase (AP) association between the environment and body sway. The posture maintenance analysis focused on estimating the amplitude and frequency characteristics of two elementary variables, which were calculated from the foot center of pressure (CoP) trajectories in the mediolateral and anteroposterior directions. The variables were trajectory of the vertical projection of the center of gravity (variable CG) and difference between the CoP and CG trajectories (variable CoP–CG). In both the absence and presence of passive tactile contact, the root mean square (RMS) values of the oscillation spectra of the two variables were the lowest in the stable visual environment and in the case of the antiphase association of the environment with body sways and the highest in the cases of the synphase association and standing with the eyes closed. Passive contact decreased body sways in both directions, and the RMSs of the spectra of the two variables decreased in all visual conditions. A greater decrease in RMS was observed for the CG variable. Body sways changed not only in amplitude, but also in frequency. Tactile contact increased the median frequencies (MFs) of the CG variable spectra calculated from the anteroposterior and mediolateral body sways. In contrast, a significant increase in MFs calculated for the CoP–CG variable was observed only for anteroposterior body sways. The results showed that passive contact of a forearm with a pliable external object, which does not provide a mechanical support for the subject, significantly improves the maintenance of the upright posture even in an unstable visual environment.     

Visual and proprioceptive contributions to postural control of upright stance in unilateral vestibulopathy

Preserving upright stance requires central integration of the sensory systems and appropriate motor output from the neuromuscular system to keep the centre of pressure (COP) within the base of support. Unilateral peripheral vestibular disorder (UPVD) causes diminished stance stability. The aim of this study was to determine the limits of stability and to examine the contribution of multiple sensory systems to upright standing in UPVD patients and healthy subjects. We hypothesized that closure of the eyes and Achilles tendon vibration during upright stance will augment the postural sway in UPVD patients more than in healthy subjects. Seventeen UPVD patients and 17 healthy subjects performed six tasks on a force plate: forwards and backwards leaning, to determine limits of stability, and upright standing with and without Achilles tendon vibration, each with eyes open and closed (with blackout glasses). The COP displacement of the patients was significantly greater in the vibration tasks than the controls and came closer to the posterior base of support boundary than the controls in all tasks. Achilles tendon vibration led to a distinctly more backward sway in both subject groups. Five of the patients could not complete the eyes closed with vibration task. Due to the greater reduction in stance stability when the proprioceptive, compared with the visual, sensory system was disturbed, we suggest that proprioception may be more important for maintaining upright stance than vision. UPVD patients, in particular, showed more difficulty in controlling postural stability in the posterior direction with visual and proprioceptive sensory disturbance.     

Vestibular humanoid postural control

Many of our motor activities require stabilization against external disturbances. This especially applies to biped stance since it is inherently unstable. Disturbance compensation is mainly reactive, depending on sensory inputs and real-time sensor fusion. In humans, the vestibular system plays a major role. When there is no visual space reference, vestibular-loss clearly impairs stance stability. Most humanoid robots do not use a vestibular system, but stabilize upright body posture by means of center of pressure (COP) control. We here suggest using in addition a vestibular sensor and present a biologically inspired vestibular sensor along with a human-inspired stance control mechanism. We proceed in two steps. First, in an introductory review part, we report on relevant human sensors and their role in stance control, focusing on own models of transmitter fusion in the vestibular sensor and sensor fusion in stance control. In a second, experimental part, the models are used to construct an artificial vestibular system and to embed it into the stance control of a humanoid. The robot’s performance is investigated using tilts of the support surface. The results are compared to those of humans. Functional significance of the vestibular sensor is highlighted by comparing vestibular-able with vestibular-loss states in robot and humans. We show that a kinematic body-space sensory feedback (vestibular) is advantageous over a kinetic one (force cues) for dynamic body-space balancing. Our embodiment of human sensorimotor control principles into a robot is more than just bionics. It inspired our biological work (neurorobotics: ‘learning by building’, proof of principle, and more). We envisage a future clinical use in the form of hardware-in-the-loop simulations of neurological symptoms for improving diagnosis and therapy and designing medical assistive devices.     

Specific and Nonspecific Visual Influences on the Stability of the Vertical Posture in Humans

We studied physiological mechanisms of vision-related stabilization of the vertical posture in humans using a stabilographic technique; spontaneous deviations of the projection of the center of gravity during quiet stance and magnitudes of the postural response to vibratory stimulation of proprioceptors of the lower leg muscles under varied conditions of visual control were measured. The stability of quiet stance, as estimated according to the root mean square value of the sagittal component of the stabilogram, was the best with eyes open. Vibration-induced postural responses were the smallest also under these conditions. Spontaneous postural sway and the amplitude of response to vibratory stimulation increased when only a central sector of visual field (20 ang. deg) was preserved and, especially, under conditions of closed eyes and horizontal inversion of visual perception using prismatic spectacles. Parallel changes in the quantitative stabilographic indices and amplitude of vibration-induced postural responses show that the intensity of the latter is probably determined by the background stiffness of the musculoskeletal system. We tried to estimate separately the contributions of the stiffness factor, on the one hand, and specific visual influences, on the other hand, by testing the parameters of quiet stance and postural responses under conditions of standing while lightly touching a support with the index finger. We found that the influence of the conditions of visual control on the stability of quiet stance while touching the support was eliminated. At the same time, the magnitude of postural responses to vibratory stimulation decreased but, nonetheless, changed with visual conditions in the same manner as when standing without additional support. We conclude that vision performs a dual function in the control of the vertical posture; it forms the basis for the spatial reference system and serves the source of information on the movements of one's body.     

Spinal Mechanisms May Provide a Combination of Intermittent and Continuous Control of Human Posture: Predictions from a Biologically Based Neuromusculoskeletal Model

Several models have been employed to study human postural control during upright quiet stance. Most have adopted an inverted pendulum approximation to the standing human and theoretical models to account for the neural feedback necessary to keep balance. The present study adds to the previous efforts in focusing more closely on modelling the physiological mechanisms of important elements associated with the control of human posture. This paper studies neuromuscular mechanisms behind upright stance control by means of a biologically based large-scale neuromusculoskeletal (NMS) model. It encompasses: i) conductance-based spinal neuron models (motor neurons and interneurons); ii) muscle proprioceptor models (spindle and Golgi tendon organ) providing sensory afferent feedback; iii) Hill-type muscle models of the leg plantar and dorsiflexors; and iv) an inverted pendulum model for the body biomechanics during upright stance. The motor neuron pools are driven by stochastic spike trains. Simulation results showed that the neuromechanical outputs generated by the NMS model resemble experimental data from subjects standing on a stable surface. Interesting findings were that: i) an intermittent pattern of muscle activation emerged from this posture control model for two of the leg muscles (Medial and Lateral Gastrocnemius); and ii) the Soleus muscle was mostly activated in a continuous manner. These results suggest that the spinal cord anatomy and neurophysiology (e.g., motor unit types, synaptic connectivities, ordered recruitment), along with the modulation of afferent activity, may account for the mixture of intermittent and continuous control that has been a subject of debate in recent studies on postural control. Another finding was the occurrence of the so-called “paradoxical” behaviour of muscle fibre lengths as a function of postural sway. The simulations confirmed previous conjectures that reciprocal inhibition is possibly contributing to this effect, but on the other hand showed that this effect may arise without any anticipatory neural control mechanism.     

Postural reactions of humans in upright stance: Dependence on different visual conditions and the level of stiffness in the ankle joints

We checked on the supposition that the magnitude of postural reactions to an unexpected postural disturbance in upright stance in humans can be determined to a considerable extent by the level of background stiffness in the ankle joints. For this purpose, we estimated changes in the joint stiffness under different conditions of visual control; these values were estimated within the period of background body oscillations (i.e., before the beginning of a compensatory motor reaction) and compared with those in the course of postural reactions evoked by vibrational stimulation of the ankle (shin) muscles. Experiments were carried where the subjects stood with open and closed eyes (OE and CE, respectively) and while standing wearing spectacles with frosted glass passing only diffuse light (DL). In the course of the tests, the subjects stood in the usual comfortable vertical position (hereafter, standard stance) or in the same position but with the possibility to lightly touch an immobile object by a finger (stance with additional support). Such technique was used to weaken the effects of CE and DL on background sways of the body and to lead these sways close to the level typical of OE conditions. The joint stiffness was estimated using an approach based on frequency filtration of oscillations of the center of pressure of the feet (CPF) that allowed us to select signals proportional to displacements of the total center of gravity (CG) of the body and to calculate the difference between oscillations of the CPF and CG (a CPF-CG variable). The CPF-CG variable is proportional to the horizontal acceleration of the CG and, therefore, can be used for estimation of the changes in stiffness in the ankle joints. Under conditions of standard stance, the usual conditions rather similarly influenced both variables (CG and CPF-CG) in the course of both background body oscillations and a postural response. The examined variables were the greatest under CE conditions, decreased under conditions of perception of DL, and became smallest with OE. At standing with additional support, the dependence of the examined variables on visual conditions disappeared within the period of background body oscillations (before the beginning of postural reactions). In this case, the magnitude of oscillations of the CPF-CG variable under CE and DL conditions decreased to the level observed at standing under OE conditions. The magnitude of CG displacements induced by vibrational stimulations of the muscles remained, nevertheless, clearly dependent on visual conditions (the same regularities were observed as in the case of standing with no additional support). Thus, our findings demonstrate that the correlation between the characteristics of postural reactions in the upright stance and the level of ankle joint stiffness is not single-valued. Neirofiziologiya/Neurophysiology, Vol. 39, No. 2, pp. 146–153, March–April, 2007.     

Effects of 20 days horizontal bed rest on maintaining upright standing posture in young persons

The effects of 20 days horizontal bed rest (BR) on postural reflex were studied by measuring fluctuation of center of gravity in the body during two legs or one leg upright standing in 10 young volunteers. The fluctuation was decided as total moving distance of the center recorded during 60sec standing on a force plate. The stability was measured by the moved area. After BR, the moving distance increased during two legs standing with open eyes (p<0.05), but statistically unchanged with closed eyes. The moving area decreased during right one-leg standing with closed eyes (p<0.05), but unchanged during left one-leg standing. Despite with open eyes the increased distance suggested that postural reflexes to maintain upright position were probably decreased by increased unsuitable feedback informations from the visual receptor deconditioning during BR. The decreased area during right one-leg standing with closed eyes also suggested that the declined standing posture reflex was probably related to more rapidly lowered functions for maintaining standing position in the dominating leg than in the other.     

Comparison of human and humanoid robot control of upright stance

There is considerable recent interest in developing humanoid robots. An important substrate for many motor actions in both humans and biped robots is the ability to maintain a statically or dynamically stable posture. Given the success of the human design, one would expect there are lessons to be learned in formulating a postural control mechanism for robots. In this study we limit ourselves to considering the problem of maintaining upright stance. Human stance control is compared to a suggested method for robot stance control called zero moment point (ZMP) compensation. Results from experimental and modeling studies suggest there are two important subsystems that account for the low- and mid-frequency (DC to 1 Hz) dynamic characteristics of human stance control. These subsystems are (1) a “sensory integration” mechanism whereby orientation information from multiple sensory systems encoding body kinematics (i.e. position, velocity) is flexibly combined to provide an overall estimate of body orientation while allowing adjustments (sensory re-weighting) that compensate for changing environmental conditions and (2) an “effort control” mechanism that uses kinetic-related (i.e., force-related) sensory information to reduce the mean deviation of body orientation from upright. Functionally, ZMP compensation is directly analogous to how humans appear to use kinetic feedback to modify the main sensory integration feedback loop controlling body orientation. However, a flexible sensory integration mechanism is missing from robot control leaving the robot vulnerable to instability in conditions where humans are able to maintain stance. We suggest the addition of a simple form of sensory integration to improve robot stance control. We also investigate how the biological constraint of feedback time delay influences the human stance control design. The human system may serve as a guide for improved robot control, but should not be directly copied because the constraints on robot and human control are different.     

Vestibular effects on posture instability evoked by moving visual environment and footing

Subjects held the vertical posture standing up on hard footing, having small degree of the freedom in the frontal plane. The stability of the vertical posture has been assessed by the standard deviations (sigma) from average amplitudes of the fluctuations of the subject's head (in frontal and sagittal planes) from conditional zero. Sinusoidal rotations of optokinetic cylinder, sinusoidal rotations of the footing, and combinations of these rotations, under phase shifts between the optokinetic cylinder and the footing, caused increase of sigma. The amplitude and velocity signal of the head deviations was transformed into low galvanic current applied to the mastoids and used as the artifical vestibular biofeedback. It was possible to reduce the value of the sigma for lateral tilts (raised in comparison with their values during stance in the dark as a result of destabilizing influence), varying coefficients of the biofeedback. At the same time, appropriate fluctuations in sagittal plane were not systematic.     

Biomechanics, evolution and upright stature

The transition from a basically quadrupedal to an upright stance must have been a critical stage in the early hominids before the appearance of Australopithecus and after a Ramaor Dryopithecine time. Two hypotheses have been postulated as to how the change occurred: 1. a gradualistic evolution from the horizontal to a more and more vertical body posture; and 2. an "either--or" position, in which our early ancestor assumed either a horizontal or a vertical posture. It is calculated that, in a static equilibrium, a semi-erect posture would be disadvantageous from the point of view of muscle forces as well as from energetic constraints. These stresses make it probable that an upright posture and carrying of objects in the hands were jointly favored by natural selection and that an intermediate stage would be short and inconclusive. The postural change would thus have occurred in a "punctuated equilibrium" manner of evolution.     

Motor pattern changes during central compensation of eyestalk posture after unilateral statolith removal in crayfish

Electromyographic recording was used to study how the activity of the eyestalk motor system is modified during the recovery of eyestalk posture following unilateral statolith removal in crayfish Procambarus clarkii Girard. Intact animals showed bilaterally balanced activity of the muscle 12 (eyecup-up muscle) in the upright body position. Body rolling caused an increase in the muscle activity on the lowered side and a decrease on the lifted side. Unilateral statolith removal caused imbalance in the bilateral muscle activity in the upright body position: the muscle 12 activity decreased tonically on the operated side and increased on the opposite side. Body rolling of the operated animal caused an increase in the muscle activity from the unbalanced level on the lowered side and a decrease on the lifted side. When the operated animal recovered its original symmetrical posture of eyestalks 14 days after operation, the muscle activity was found on both sides to return to the previous level observed before statolith removal, regardless of the post-operative condition in which the animal was maintained. In those animals that did not recover the original eyestalk posture, the unbalanced activity of bilateral muscles that was caused by unilateral statolith removal remained unchanged. The results indicate that the recovery of eyestalk posture is based on restoration of the original activity balance, rather than on fixation of the operation-induced activity imbalance, among bilaterally homologous sets of muscles in the course of central compensation.     

Influence of a movable support under one leg on human vertical posture during standing with asymmetrical load on legs

Changes in the vertical posture maintenance were studied when the legs were placed on supports of different degrees of mobility and part of the body weight was voluntarily transferred to one leg. The aim of these experiments was to explore how the mobility of support under the feet affects the balance and how this effect depends on the load distribution between the legs during standing. When both legs were on rigid immovable supports, the vertical posture was maintained by control of the center of pressure (CP) on both legs. When the subject transferred the weight to one foot, the posture was maintained mainly due to the control of CP of the loaded leg. When the legs were on supports of different degrees of mobility, the balance was maintained by the leg on the immovable support. This result was observed both when the subject stood with symmetrical load on the legs and when the load was transferred to one leg. Even when the leg was unloaded but placed on the immovable support, its CP moved more compared to the CP of the loaded leg on a movable support. The results obtained show that the support mobility is a factor that determines the mechanisms of posture maintenance, and this factor is more significant than load distribution between the legs. Thus, the upright posture is maintained with the physical properties of support under the feet taken into account.     

Trunk muscle electromyography and whole body vibration

By measuring the electromyographic (EMG) activity of the paraspinal muscles, we have estimated the average and peak-to-peak torque imposed on the spine during whole body vibration. Six subjects had surface electrodes placed on their erector spinae muscles at the L3 level. The EMG-torque relationship was estimated by having each subject perform isometric horizontal pulls in an upright seated posture. The subject was then vibrated vertically and sinusoidally in a controlled, flexed, slightly lordotic seated posture, in 1 Hz increments from 3 to 10 Hz at a 0.1 g RMS seat acceleration level. Between vibration readings taken at each frequency, a static reading was also taken with the subject maintaining the same posture. The entire vibration-static 3-10 Hz test was repeated for reliability purposes. Specialized digital signal processing techniques were developed for the EMG signals to enhance the measured cyclic muscle activity and to allow automatic measurement of the time relationship between the mechanical displacement and the estimated torque. We found significantly more average and peak-to-peak estimated torque at almost all frequencies for vibration vs static sitting.     

Mechanisms of reference posture correction in the system of upright posture control

It was earlier shown that ultraslow tilts of the support under quiet standing conditions evoke an unusual response reflecting the operation of compensatory mechanisms: postural sway is a superposition of postural oscillations typical of quiet standing and greater, slower inclinations of the body caused by the tilt. This may be explained by the presence of two hierarchical levels of upright posture control: real-time control compensates for small deviations of the body from the reference posture prescribed by presetting control. Mathematical simulation methods have been used to study the mechanisms of reference posture control. The results are compared with available experimental data. It is demonstrated that the reference posture can be corrected according to the gravitational vertical with the use of a kinesthetic reference alone. It is hypothesized that, when correcting the reference posture, the nervous system “assumes” the support to be immobile. The afferent input from sole pressure receptors is an important factor in reference posture correction. The advantages of the putative two-level control over control based on an explicit internal model are discussed.     

Models of Postural Control: Shared Variance in Joint and COM Motions

This paper investigated the organization of the postural control system in human upright stance. To this aim the shared variance between joint and 3D total body center of mass (COM) motions was analyzed using multivariate canonical correlation analysis (CCA). The CCA was performed as a function of established models of postural control that varied in their joint degrees of freedom (DOF), namely, an inverted pendulum ankle model (2DOF), ankle-hip model (4DOF), ankle-knee-hip model (5DOF), and ankle-knee-hip-neck model (7DOF). Healthy young adults performed various postural tasks (two-leg and one-leg quiet stances, voluntary AP and ML sway) on a foam and rigid surface of support. Based on CCA model selection procedures, the amount of shared variance between joint and 3D COM motions and the cross-loading patterns we provide direct evidence of the contribution of multi-DOF postural control mechanisms to human balance. The direct model fitting of CCA showed that incrementing the DOFs in the model through to 7DOF was associated with progressively enhanced shared variance with COM motion. In the 7DOF model, the first canonical function revealed more active involvement of all joints during more challenging one leg stances and dynamic posture tasks. Furthermore, the shared variance was enhanced during the dynamic posture conditions, consistent with a reduction of dimension. This set of outcomes shows directly the degeneracy of multivariate joint regulation in postural control that is influenced by stance and surface of support conditions.     

In vivo length and shortening of canine diaphragm with body postural change

Using sonomicrometry, we measured the in vivo tidal shortening and velocity of shortening of the costal and crural segments of the diaphragm in the anesthetized dog in the supine, upright, tailup, prone, and lateral decubitus postures. When compared with the supine position, end-expiratory diaphragmatic length varied by less than 11% in all postures, except the upright. During spontaneous breathing, the tidal shortening and the velocity of shortening of the crural segment exceeded that of the costal segment in all postures except the upright and was maximal for both segments in the prone posture. We noted the phasic integrated electromyogram to increase as the end-expiratory length of the diaphragm shortened below and to decrease as the diaphragm lengthened above its optimal length. This study shows that the costal and crural segments have a different quantitative behavior with body posture and both segments show a compensation in neural drive to changes in resting length.     

Muscle contributions to support during gait in an individual with post-stroke hemiparesis

Walking requires coordination of muscles to support the body during single stance. Impaired ability to coordinate muscles following stroke frequently compromises walking performance and results in extremely low walking speeds. Slow gait in post-stroke hemiparesis is further complicated by asymmetries in lower limb muscle excitations. The objectives of the current study were: (1) to compare the muscle coordination patterns of an individual with flexed stance limb posture secondary to post-stroke hemiparesis with that of healthy adults walking very slowly, and (2) to identify how paretic and non-paretic muscles provide support of the body center of mass in this individual. Simulations were generated based on the kinematics and kinetics of a stroke survivor walking at his self-selected speed (0.3 m/s) and of three speed-matched, healthy older individuals. For each simulation, muscle forces were perturbed to determine the muscles contributing most to body weight support (i.e., height of the center of mass during midstance). Differences in muscle excitations and midstance body configuration caused paretic and non-paretic ankle plantarflexors to contribute less to midstance support than in healthy slow gait. Excitation of paretic ankle dorsiflexors and knee flexors during stance opposed support and necessitated compensation by knee and hip extensors. During gait for an individual with post-stroke hemiparesis, adequate body weight support is provided via reorganized muscle coordination patterns of the paretic and non-paretic lower limbs relative to healthy slow gait.     

Human Postural Responses to Vibratory Stimulation of Calf Muscles under Conditions of Visual Inversion

The authors studied postural responses to bilateral vibratory stimulation (70 Hz, 1 mm, 2 s) of the calf triceps proprioceptors or anterior tibial muscles. Anteroposterior body tilts evoked by vibration were recorded by stabilography. The authors compared the values of postural responses under various conditions of visual control, namely, with normal vision, eyes closed, right–left inversion of the visual space by prismatic spectacles, central vision, and diffuse light. Visual inversion influenced the subjects' proprioceptive postural responses. The amplitude of vibration-evoked shifts of the feet pressure center was minimal with eyes open and significantly increased with eyes closed and inverted vision. Postural responses with visual inversion were significantly stronger than with eyes closed. Since inversion spectacles enabled a subject to see only the central part of the visual field (20°), the reference point was the condition of central vision, i.e., spectacles with same visual angle and without prisms. Postural responses were significantly weaker under these conditions than with visual inversion and eyes closed. Visual field inversion by prismatic spectacles made it impossible to use visual information for stabilizing the human upright posture and, moreover, destabized it. True, this holds only for a randomized experimental protocol, which prevents adaptation to prisms.