Comparative neurobiology of postural control

In recent years, studies of nervous mechanisms for the control of body posture have been performed on animal models of different complexity - cat, rabbit, lamprey and the mollusc Clione. These studies have greatly expanded our knowledge of how the control system operates, how the system can change the stabilized body orientation and how the postural functions are distributed within different parts of the CNS. For simpler animal models, the postural network has been analyzed in considerable detail and main cell types and their interactions have been identified.     

Do Adolescent Idiopathic Scoliosis (AIS) Neglect Proprioceptive Information in Sensory Integration of Postural Control?

Introduction

It has been reported that AIS rely much more on ankle proprioception to control the amplitude of the balance control commands as compared to age-matched healthy adolescents. Our hypothesis was that AIS do not neglect proprioceptive information to control posture probably because of their vestibular deficits. We investigated the proprioceptive contribution to postural control in AIS which expresses spinal deformity during a crucial transitional period of ontogenesis.

Methods

10 adolescents with idiopathic scoliosis (AIS) with moderate spinal deformity (10° < Cobb Angle >35°) and 10 control adolescents (CA) had to maintain vertical stance while very slow oscillations in the frontal plane (below the detection threshold of the semicircular canal system) were applied to the support with the eyes open and closed. Postural orientation and segmental stabilisation were analysed at head, shoulder, trunk and pelvis levels.

Results

Scoliosis did not affect vertical orientation control and segmental stabilization strategies. Vision improves postural control in both CA and AIS, which seem more dependent on visual cues than adults.

Conclusions

AIS as CA were unable to control efficiently their postural orientation on the basis of the proprioceptive cues, the only sensory information available in the EC situation, whereas in the same condition healthy young adults present no difficulty to achieve the postural control. This suggests that AIS as CA transitory neglect proprioceptive information to control their posture. These results and previous studies suggest the existence of different afferent pathways for proprioceptive information subserving different parts in sensory integration of postural control. We conclude that the static proprioceptive system is not affected by the idiopathic scoliosis, while the dynamic proprioceptive system would be mainly affected.     

Evaluation of time-to-contact measures for assessing postural stability

Postural stability has traditionally been examined through spatial measures of the center of mass (CoM) or center of pressure (CoP), where larger amounts of CoM or CoP movements are considered signs of postural instability. However, for stabilization, the postural control system may utilize additional information about the CoM or CoP such as velocity, acceleration, and the temporal margin to a stability boundary. Postural time-to-contact (TtC) is a variable that can take into account this additional information about the CoM or CoP. Postural TtC is the time it would take the CoM or CoP, given its instantaneous trajectory, to contact a stability boundary. This is essentially the time the system has to reverse any perturbation before stance is threatened. Although this measure shows promise in assessing postural stability, the TtC values derived between studies are highly ambiguous due to major differences in how they are calculated. In this study, various methodologies used to assess postural TtC were compared during quiet stance and induced-sway conditions. The effects of the different methodologies on TtC values will be assessed, and issues regarding the interpretation of TtC data will also be discussed.     

Postural control system

The postural control system has two main functions: first, to build up posture against gravity and ensure that balance is maintained; and second, to fix the orientation and position of the segments that serve as a reference frame for perception and action with respect to the external world. This dual function of postural control is based on four components: reference values, such as orientation of body segments and position of the center of gravity (an internal representation of the body or postural body scheme); multisensory inputs regulating orientation and stabilization of body segments; and flexible postural reactions or anticipations for balance recovery after disturbance, or postural stabilization during voluntary movement. The recent data related to the organization of this system will be discussed in normal subjects (during ontogenesis), the elderly and in patients with relevant deficits.     

Predicting the dynamic postural control response from quiet-stance behavior in elderly adults

Human postural sway, as measured by fluctuations of the center of pressure (COP) under the feet of a quietly standing individual, can be characterized as a stochastic process. The fluctuation-dissipation theorem (FDT) provides a linear relationship between the fluctuations of a quasi-static, stochastic system to the same system's relaxation to equilibrium following a perturbation. We applied a similar linear relationship, based on the FDT, to the human postural control system to explore whether anterior-posterior (AP) fluctuations of the COP during quiet stance can be used to predict the AP response of the postural control system to a weak posteriorly directed mechanical perturbation (tug or pull at the waist). We tested 10 healthy elderly (mean age of 69yr) and 10 healthy young (mean age of 25yr) adult subjects. We found that this linear relationship was applicable to the postural control system of all 10 young and eight of the 10 elderly adult subjects. These results suggest that it is possible to predict an individual's dynamic response to a mild perturbation using quiet-stance data, regardless of age. The existence of this FDT-based linear relationship with respect to the human postural control system suggests that, for a given individual, the postural control system may use the same control mechanisms during quiet stance and mild-perturbation conditions, regardless of age.     

Effect of a dual task on postural control in dyslexic children

Several studies have examined postural control in dyslexic children; however, their results were inconclusive. This study investigated the effect of a dual task on postural stability in dyslexic children. Eighteen dyslexic children (mean age 10.3±1.2 years) were compared with eighteen non-dyslexic children of similar age. Postural stability was recorded with a platform (TechnoConcept®) while the child, in separate sessions, made reflex horizontal and vertical saccades of 10° of amplitude, and read a text silently. We measured the surface and the mean speed of the center of pressure (CoP). Reading performance was assessed by counting the number of words read during postural measures. Both groups of children were more stable while performing saccades than while reading a text. Furthermore, dyslexic children were significantly more unstable than non-dyslexic children, especially during the reading task. Finally, the number of words read by dyslexic children was significantly lower than that of non-dyslexic children and, in contrast to the non-dyslexic children. In line with the U-shaped non-linear interaction model, we suggest that the attention consumed by the reading task could be responsible for the loss of postural control in both groups of children. The postural instability observed in dyslexic children supports the hypothesis that such children have a lack of integration of multiple sensorimotor inputs.     

Reweighting of sensory inputs to control quiet standing in children from 7 to 11 and in adults

How sensory organization for postural control matures in children is not clear at this time. The present study examined, in children aged 7 to 11 and in adults, the postural control modifications in quiet standing when somatosensory inputs from the ankle were disturbed. Since the reweighting of sensory inputs is not mature before 10, we hypothesized that postural stability was more affected in children than in adults when somatosensory inputs were altered and that this postural instability decreased as age increased during childhood. 37 children aged 7 to 11 years and 9 adults participated in the experiments. The postural task was a semi-tandem position with the right foot in front of the left one. Postural performance was measured by means of a force platform. Two experimental conditions were presented to the participants to maintain quiet standing: With or without altered somatosensory inputs (i.e., with or without ankles vibration). Results showed that postural stability--and thus how the reweighting process of the visual/somatosensory inputs matured--increased non-monotonically between 7 years of age and adult age: There was a linear improvement of postural stability from 7 to 10, followed by a more steady behaviour between 10 and 11 and then postural stability increased to reach the adults' level of performance.     

Control of motoneuron function and muscle tone during REM sleep, REM sleep behavior disorder and cataplexy/narcolepsy

REM sleep triggers a potent suppression of postural muscle tone - i.e., REM atonia. However, motor control during REM sleep is paradoxical because overall brain activity is maximal, but motor output is minimal. The skeletal motor system remains quiescent during REM sleep because somatic motoneurons are powerfully inactivated. Determining the mechanisms triggering loss of motoneuron function during REM sleep is important because breakdown in REM sleep motor control underlies sleep disorders such as REM sleep behavior disorder (RBD) and cataplexy/narcolepsy. For example, RBD is characterized by dramatic REM motor activation resulting in dream enactment and subsequent patient injury. In contrast, cataplexy a pathognomonic symptom of narcolepsy - is caused by the involuntary onset of REM-like atonia during wakefulness. This review highlights recent work from my laboratory that examines how motoneuron function is lost during normal REM sleep and it also identifies potential biochemical mechanisms underlying abnormal motor control in both RBD and cataplexy. First, I show that both GABAB and GABAA/glycine mediated inhibition of motoneurons is required for generating REM atonia. Next, I show that impaired GABA and glycine neurotransmission triggers the cardinal features of RBD in a transgenic mouse model. Last, I show that loss of an excitatory noradrenergic drive onto motoneurons is, at least in part, responsible for the loss of postural muscle tone during cataplexy in narcoleptic mice. Together, this research indicates that multiple transmitters systems are responsible for regulating postural muscle tone during REM sleep, RBD and cataplexy.     

Does whole-body vibration training have acute residual effects on postural control ability of elderly women?

The purpose of this study was to investigate acute residual effects of a single vibration session on balance control in a group of elderly women. Several studies, in fact, have shown that whole-body vibration (WBV) training may improve balance in the elderly, but possible side effects of acute exposure to WBV, such as temporary reduction of balance control ability because of perturbations of the vestibular system, have not been investigated. Twenty-two healthy elderly women (71.8 ± 4.7 years of age) were trained with a 9.5-minute bout of static and dynamic knee-extensor exercises executed on a vibrating platform (Well-net Vibe Revolution). The vibration frequency was set at 35 Hz. A subgroup of 14 subjects performed the same exercise protocol also without the vibrations to discriminate between vibration and exercise effects. Balance control ability was assessed through computerized posturography: a force plate (Bertec Co, Columbus, OH, USA) was used to measure the center of pressure trajectories during 4 different experimental trials: before, immediately after, 15 minutes after, and 60 minutes after the training. A set of postural parameters, typically adopted to assess elderly subjects, was then computed and 2-way analysis of variance was used to determine differences between values found in the 4 postural tests (level of significance p = 0.05) in the 2 groups. The results showed no significant variations in the postural parameters recorded during the 4 sessions. A significant group effect was found for 2 postural parameters, with no interaction between the 2 factors. In conclusion, the proposed single bout of WBV does not induce dangerous acute effects on elderly women balance control ability and could be safely administered as part of a long-term intervention program.     

Evaluation of posture signal using entropy analysis and fractal dimension in adults with Down syndrome

The aim of this study was to explore new techniques in analysing postural control using nonlinear time-series analysis and to relate these results with the clinical knowledge on the postural system in Down syndrome (DS) subjects. In order to achieve the goal, we analysed the time domain and the frequency domain behaviour, the fractal dimension and the entropy of the centre of pressure signal in both directions during quiet standing in 35 participants with DS, comparing the results with a control population. DS patients evidenced a lack in postural control in anterior–posterior direction due to the impairment both in the high organisation and synergies and in the impairments due to ligament laxity and hypotonia. Maintaining posture is a task achieved by the integration of visual, vestibular and somatosensory receptors and the dynamical nature of this signal gives fundamental data about the lack of postural control in specific pathological condition.     

Comparing internal models of the dynamics of the visual environment

It is well known that the human postural control system responds to motion of the visual scene, but the implicit assumptions it makes about the visual environment and what quantities, if any, it estimates about the visual environment are unknown. This study compares the behavior of four models of the human postural control system to experimental data. Three include internal models that estimate the state of the visual environment, implicitly assuming its dynamics to be that of a linear stochastic process (respectively, a random walk, a general first-order process, and a general second-order process). In each case, all of the coefficients that describe the process are estimated by an adaptive scheme based on maximum likelihood. The fourth model does not estimate the state of the visual environment. It adjusts sensory weights to minimize the mean square of the control signal without making any specific assumptions about the dynamic properties of the environmental motion.We find that both having an internal model of the visual environment and its type make a significant difference in how the postural system responds to motion of the visual scene. Notably, the second-order process model outperforms the human postural system in its response to sinusoidal stimulation. Specifically, the second-order process model can correctly identify the frequency of the stimulus and completely compensate so that the motion of the visual scene has no effect on sway. In this case the postural control system extracts the same information from the visual modality as it does when the visual scene is stationary. The fourth model that does not simulate the motion of the visual environment is the only one that reproduces the experimentally observed result that, across different frequencies of sinusoidal stimulation, the gain with respect to the stimulus drops as the amplitude of the stimulus increases but the phase remains roughly constant. Our results suggest that the human postural control system does not estimate the state of the visual environment to respond to sinusoidal stimuli.     

Challenging Postural Tasks Increase Asymmetry in Patients with Parkinson’s Disease

The unilateral predominance of Parkinson’s disease (PD) symptoms suggests that balance control could be asymmetrical during static tasks. Although studies have shown that balance control asymmetries exist in patients with PD, these analyses were performed using only simple bipedal standing tasks. Challenging postural tasks, such as unipedal or tandem standing, could exacerbate balance control asymmetries. To address this, we studied the impact of challenging standing tasks on postural control asymmetry in patients with PD. Twenty patients with PD and twenty neurologically healthy individuals (control group) participated in this study. Participants performed three 30s trials for each postural task: bipedal, tandem adapted and unipedal standing. The center of pressure parameter was calculated for both limbs in each of these conditions, and the asymmetry between limbs was assessed using the symmetric index. A significant effect of condition was observed, with unipedal standing and tandem standing showing greater asymmetry than bipedal standing for the mediolateral root mean square (RMS) and area of sway parameters, respectively. In addition, a group*condition interaction indicated that, only for patients with PD, the unipedal condition showed greater asymmetry in the mediolateral RMS and area of sway than the bipedal condition and the tandem condition showed greater asymmetry in the area of sway than the bipedal condition. Patients with PD exhibited greater asymmetry while performing tasks requiring postural control when compared to neurologically healthy individuals, especially for challenging tasks such as tandem and unipedal standing.     

Effect of hip and ankle muscle fatigue on unipedal postural control

Fatigue and deficits in postural control may predispose musculoskeletal injury. The purpose of this study was to examine the effects of fatigue at the hip and ankle during frontal plane movements on postural control during single-leg stance. Thirteen healthy volunteers completed two testing sessions 1 week apart consisting of isokinetic fatigue of the frontal plane movers of either the ankle or hip with measures of static unipedal postural control taken before and after fatigue. Postural control was assessed during three 30-s trials of unilateral stance with eyes open before and after the fatigue protocol at each testing session. Mean center of pressure (COP) excursion velocity in the sagittal and frontal planes was compared between pre- and post-fatigue across the two joints. Fatigue of the hip musculature led to postural control impairments in the frontal and sagittal planes, while fatigue of the ankle musculature did not significantly impair postural control in either plane. Our results suggest that there is a greater effect of localized fatigue of the frontal plane movers of the hip compared to the ankle on maintenance of a postural control in single-leg stance.     

Effect of tongue position on postural stability during quiet standing in healthy young males

Abstract

Background and aims: Role of the neck and jaw sensory motor system in control of body balance has been established. Tongue is an integral part of jaw sensory motor system and helps in execution of purposeful and precise motor tasks like eating, drinking and speaking. The purpose of this study was to evaluate the possible effects of tongue position on the postural control system.

Materials and method: We compared the mean center of gravity (COG) velocity during quiet standing on an unstable surface with eyes closed during two test conditions: (i) with habitual jaw resting position and (ii) with instructed tongue positioned against the upper incisors. One hundred and sixteen normal healthy male subjects (average age 31.56?±?8.51 years and height 170.86?±?7.26?cm) participated in the study. Their COG velocity (deg/s) was measured using the NeuroCom® Balance Master version 8.5.0 (Clackamas, OR, USA).

Results and conclusions: The results show that COG velocity decreased significantly while tongue was positioned against upper incisors in comparison to the habitual jaw resting position. Our findings suggest that the tongue positioning can modulate postural control mechanisms. Tongue positioning against the upper incisors can enhance the postural stability during upright standing on an unstable surface and in the absence of vision in healthy young adults. Our findings can be of value for evaluation and rehabilitation protocols for postural control dysfunction.     

The role of anticipatory postural adjustments in compensatory control of posture: 1. Electromyographic analysis

Anticipatory (APAs) and compensatory (CPAs) postural adjustments are the two principal mechanisms that the central nervous system uses to maintain equilibrium while standing. We studied the role of APAs in compensatory postural adjustments. Eight subjects were exposed to external predictable and unpredictable perturbations induced at the shoulder level, while standing with eyes open and closed. Electrical activity of leg and trunk muscles was recorded and analyzed during four epochs representing the time duration typical for anticipatory and compensatory postural control. No anticipatory activity of the trunk and leg muscles was seen in the case of unpredictable perturbations; instead, significant compensatory activation of muscles was observed. When the perturbations were predictable, strong anticipatory activation was seen in all the muscles: such APAs were associated with significantly smaller compensatory activity of muscles and COP displacements after the perturbations.The outcome of the study highlights the importance of APAs in control of posture and points out the existence of a relationship between the anticipatory and the compensatory components of postural control. It also suggests a possibility to enhance balance control by improving the APAs responses during external perturbations.     

A robotic device for understanding neuromechanical interactions during standing balance control

Postural stability in standing balance results from the mechanics of body dynamics as well as active neural feedback control processes. Even when an animal or human has multiple legs on the ground, active neural regulation of balance is required. When the postural configuration, or stance, changes, such as when the feet are placed further apart, the mechanical stability of the organism changes, but the degree to which this alters the demands on neural feedback control for postural stability is unknown. We developed a robotic system that mimics the neuromechanical postural control system of a cat in response to lateral perturbations. This simple robotic system allows us to study the interactions between various parameters that contribute to postural stability and cannot be independently varied in biological systems. The robot is a 'planar', two-legged device that maintains compliant balance control in a variety of stance widths when subject to perturbations of the support surface, and in this sense reveals principles of lateral balance control that are also applicable to bipeds. Here we demonstrate that independent variations in either stance width or delayed neural feedback gains can have profound and often surprisingly detrimental effects on the postural stability of the system. Moreover, we show through experimentation and analysis that changing stance width alters fundamental mechanical relationships important in standing balance control and requires a coordinated adjustment of delayed feedback control to maintain postural stability.     

Independent activation in adjacent lumbar extensor muscle compartments

The purpose of this study was to examine compartmentalization in human lumbar spine extensors. Structure and innervation of these muscles would suggest the possibility of more segmentally specific biomechanical functions than have been found in previous studies examining muscle activation patterns during simple spine bending and twisting tasks. We selected specialized tasks to more effectively investigate the degree of independent control possible within lumbar spine extensors. We recorded surface electromyograms (SEMG) from the right posterior lumbar region during performance of two segmentally specific bellydance skills by seven novice and five trained subjects. These movements were performed at two frequencies (0.5 and 1Hz). Cross-correlations were performed between pairs of rectified, low-pass filtered (6Hz) SEMG signals to determine temporal lags between rhythmic bursts. Results showed a difference in the timing of muscle activation above and below the third lumbar vertebra. Temporal asynchrony was independent of either skill level or tempo, suggesting a hard-wired capacity for independent control of adjacent muscle compartments. The results have implications for understanding trunk control in the context of postural stability and postural adaptation during locomotion, as well as for lower back functional assessment and rehabilitation.     

Postural Strategies and Sensory Integration: No Turning Point between Childhood and Adolescence

In this study, we investigated the sensory integration to postural control in children and adolescents from 5 to 15 years of age. We adopted the working hypothesis that considerable body changes occurring during these periods may lead subjects to under-use the information provided by the proprioceptive pathway and over-use other sensory systems such as vision to control their orientation and stabilize their body. It was proposed to determine which maturational differences may exist between the sensory integration used by children and adolescents in order to test the hypothesis that adolescence may constitute a specific phase in the development of postural control. This hypothesis was tested by applying an original protocol of slow oscillations below the detection threshold of the vestibular canal system, which mainly serves to mediate proprioceptive information, to the platform on which the subjects were standing. We highlighted the process of acquiring an accurate sensory and anatomical reference frame for functional movement. We asked children and adolescents to maintain a vertical stance while slow sinusoidal oscillations in the frontal plane were applied to the support at 0.01 Hz (below the detection threshold of the semicircular canal system) and at 0.06 Hz (above the detection threshold of the semicircular canal system) with their eyes either open or closed. This developmental study provided evidence that there are mild differences in the quality of sensory integration relative to postural control in children and adolescents. The results reported here confirmed the predominance of vision and the gradual mastery of somatosensory integration in postural control during a large period of ontogenesis including childhood and adolescence. The youngest as well as the oldest subjects adopted similar qualitative damping and segmental stabilization strategies that gradually improved with age without reaching an adult''s level. Lastly, sensory reweighting for postural strategies as assessed by very slow support oscillations presents a linear development without any qualitative turning point between childhood and adolescence.     

Functional Synergies Underlying Control of Upright Posture during Changes in Head Orientation

Background

Studies of human upright posture typically have stressed the need to control ankle and hip joints to achieve postural stability. Recent studies, however, suggest that postural stability involves multi degree-of-freedom (DOF) coordination, especially when performing supra-postural tasks. This study investigated kinematic synergies related to control of the body’s position in space (two, four and six DOF models) and changes in the head’s orientation (six DOF model).

Methodology/Principal Findings

Subjects either tracked a vertically moving target with a head-mounted laser pointer or fixated a stationary point during 4-min trials. Uncontrolled manifold (UCM) analysis was performed across tracking cycles at each point in time to determine the structure of joint configuration variance related to postural stability or tracking consistency. The effect of simulated removal of covariance among joints on that structure was investigated to further determine the role of multijoint coordination. Results indicated that cervical joint motion was poorly coordinated with other joints to stabilize the position of the body center of mass (CM). However, cervical joints were coordinated in a flexible manner with more caudal joints to achieve consistent changes in head orientation.

Conclusions/Significance

An understanding of multijoint coordination requires reference to the stability/control of important performance variables. The nature of that coordination differs depending on the reference variable. Stability of upright posture primarily involved multijoint coordination of lower extremity and lower trunk joints. Consistent changes in the orientation of the head, however, required flexible coordination of those joints with motion of the cervical spine. A two-segment model of postural control was unable to account for the observed stability of the CM position during the tracking task, further supporting the need to consider multijoint coordination to understand postural stability.     

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.