The effect of voluntary lateral trunk bending on balance recovery following multi-directional stance perturbations

Stabilising shifts of the centre of mass (COM) are observed during balance recovery when subjects simultaneously execute voluntary unilateral knee flexion or unilateral arm raising. Here, we examined whether voluntary lateral trunk bending provided more beneficial stabilising effects, and how motor programs of balance corrections are combined with those of the focal voluntary action. The upright balance of 24 healthy young subjects (19–33 years of age) was perturbed using multi-directional rotations of the support-surface. The perturbations consisted of combined pitch and roll rotations (7.5° and 60°/s) presented randomly in six different directions. Three conditions were tested: perturbation of stance only (PO); combined balance perturbation and cued uphill bending of the trunk (CONT); and combined perturbation and cued downhill bending of the trunk (IPS). For comparison, subjects were required to perform trunk bending alone (TO). Outcome measures were biomechanical responses and surface EMG activity of several muscles. Calculated predicted outcomes (PO + TO) were compared with combined measures (CONT or IPS). CONT trunk bending uphill showed two phases of benefit in balance recovery for laterally but, in contrast to voluntary knee bending, not for posterior directed components of the perturbations. IPS trunk bending had negative effects on balance. Early balance correcting muscle responses were marginally greater than PO responses. Prominent secondary balance correcting responses, having a similar timing as voluntary responses observed under TO conditions, were seen under CONT only in trunk muscles. These, and later stabilising, responses had amplitudes as expected from PO + TO conditions being significantly greater than PO responses. The ability with which different muscle synergies for balance corrections and voluntary trunk bending were integrated into one indicates a flexible adjustment of the CNS programs to the demands of both tasks.     

Vestibular influences on human postural control in combinations of pitch and roll planes reveal differences in spatiotemporal processing

The present study examined the influence of bilateral peripheral vestibular loss (BVL) in humans on postural responses to multidirectional surface rotations in the pitch and roll planes. Specifically, we examined the effects of vestibular loss on the directional sensitivity, timing, and amplitude of early stretch, balance correcting, and stabilizing reactions in postural leg and trunk muscles as well as changes in ankle torque and trunk angular velocity following multidirectional rotational perturbations of the support surface. Fourteen normal healthy adults and five BVL patients stood on a dual axis rotating platform which rotated 7.5° at 50°/s through eight different directions of pitch and roll combinations separated by 45°. Directions were randomized within a series of 44 perturbation trials which were presented first with eyes open, followed by a second series of trials with eyes closed. Vestibular loss did not influence the range of activation or direction of maximum sensitivity for balance correcting responses (120–220 ms). Response onsets at approximately 120 ms were normal in tibialis anterior (TA), soleus (SOL), paraspinals (PARAS), or quadriceps muscles. Only SOL muscle activity demonstrated a 38- to 45-ms delay for combinations of forward (toe-down) and roll perturbations in BVL patients. The amplitude of balance correcting responses in leg muscles between 120 and 220 ms was, with one exception, severely reduced in BVL patients for eyes open and eyes closed conditions. SOL responses were decreased bilaterally for toe-up and toe-down perturbations, but more significantly reduced in the downhill (load-bearing) leg for combined roll and pitch perturbations. TA was significantly reduced bilaterally for toe-up perturbations, and in the downhill leg for backward roll perturbations. Forward perturbations, however, elicited significantly larger TA activity in BVL between 120 and 220 ms compared to normals, which would act to further destabilize the body. As a result of these changes in response amplitudes, BVL patients had reduced balance correcting ankle torque between 160 and 260 ms and increased torque between 280 and 380 ms compared to normals. There were no differences in the orientation of the resultant ankle torque vectors between BVL and normals, both of which were oriented primarily along the pitch plane. For combinations of backward (toe-up) and roll perturbations BVL patients had larger balance correcting and stabilizing reactions (between 350 and 700 ms) in PARAS than normals and these corresponded to excessive trunk pitch and roll velocities. During roll perturbations, trunk velocities in BVL subjects after 200 ms were directed along directions different from those of normals. Furthermore, roll instabilities appeared later than those of pitch particularly for backward roll perturbations. The results of the study show that combinations of roll and pitch surface rotations yield important spatiotemporal information, especially with respect to trunk response strategies changed by BVL which are not revealed by pitch plane perturbations alone. Our results indicate that vestibular influences are earlier for the pitch plane and are directed to leg muscles, whereas roll control is later and focused on trunk muscles. Electronic Publication     

The influence of knee rigidity on balance corrections: a comparison with responses of cerebellar ataxia patients

Knee rigidity due to aging or disease is associated with falls. A causal relationship between instability and knee rigidity has not been established. Here, we examined whether insufficient knee movement due to knee rigidity could underlie poor balance control in patients. We addressed this by examining the effect of artificially “locking” the knees on balance control in 18 healthy subjects, tested with and without individually fitted knee casts on both legs. Subjects were exposed to sudden rotations of a support surface in six different directions. The primary outcome measure was body centre of mass (COM) movement, and secondary outcome measures included biomechanical responses of the legs, pelvis and trunk. Knee casts caused increased backward COM movement for backward perturbations and decreased vertical COM movement for forward perturbations, and caused little change in lateral COM movement. At the ankles, dorsiflexion was reduced for backward perturbations. With knee casts, there was less uphill hip flexion and more downhill hip flexion. A major difference with knee casts was a reversed pelvis pitch movement and an increased forward trunk motion. These alterations in pitch movement strategies and COM displacements were similar to those we have observed previously in patients with knee rigidity, specifically those with spinocerebellar ataxia (SCA). Pelvis roll and uphill arm abduction were also increased with the casts. This roll movement strategy and minor changes in lateral COM movement were not similar to observations in patients. We conclude that artificial knee rigidity increases instability, as reflected by greater posterior COM displacement following support surface tilts. Healthy controls with knee casts used a pitch movement strategy similar to that of SCA patients to offset their lack of knee movement in regaining balance following multidirectional perturbations. This similarity suggests that reduced knee movements due to knee rigidity may contribute to sagittal plane postural instability in SCA patients and possibly in other patient groups. However in the roll plane, healthy controls rapidly compensate by adjusting arm movements and hip flexion to offset the effects of knee rigidity.     

Directional sensitivity of stretch reflexes and balance corrections for normal subjects in the roll and pitch planes

A large body of evidence has been collected which describes the response parameters associated with automatic balance corrections in man to perturbations in the pitch plane. However, perturbations to human stance can be expected from multiple directions. The purpose of the present study was to describe the directional sensitivities of muscle responses re-establishing disturbed stance equilibrium in normal subjects. The contributions of stretch reflex and automatic balance-correcting responses to balance control, and concomitant biomechanical reactions, were examined for combinations of pitch and roll perturbations of the support surface. More specifically, muscle responses, initial head accelerations and trunk velocities were analyzed with the intention of identifying possible origins of directionally specific triggering signals and to examine how sensory information is used to modulate triggered balance corrections with respect to direction. Fourteen healthy adults were required to stand on a dual-axis rotating platform capable of delivering rotational perturbations with constant amplitude (7.5°) and velocity (50°/s) through multiple directions in the pitch and roll planes. Each subject was randomly presented with 44 support surface rotations through 16 different directions separated by 22.5° first under eyes-open, and then, for a second identical set of rotations, under eyes-closed conditions. Bilateral muscle activities from tibialis anterior, soleus, lateral quadriceps and paraspinals were recorded, averaged across direction, and areas calculated over intervals with significant bursts of activity. Trunk angular velocity and ankle torque data were averaged over intervals corresponding to significant biomechanical events. Stretch reflex (intervals of 40–100, 80–120 ms) and automatic balance-correcting responses (120–220, 240–340 ms) in the same muscle were sensitive to distinctly different directions. The directions of the maximum amplitude of balance-correcting activity in leg muscles were oriented along the pitch plane, approximately 180° from the maximum amplitude of stretch responses. Ankle torques for almost all perturbation directions were also aligned along the pitch plane. Stretch reflexes in paraspinal muscles were tuned along the 45° plane but at 90° to automatic balance corrections and 180° to unloading responses in the same muscle. Stretch reflex onsets in paraspinal muscles were observed at 60 ms, as early as those of soleus muscles. In contrast, unloading reflexes in released paraspinal muscles were observed at 40 ms for perturbations which caused roll of the trunk towards the recorded muscle. Onsets of trunk roll velocities were earlier and more rapid than those observed for pitch velocities. Trunk pitch occurred for pure roll directions but not vice versa. When considered together, early stretch and unloading of paraspinals, and concomitant roll and pitch velocities of the trunk requiring a roll-and-pitch-based hip torque strategy, bring into question previous hypotheses of an ankle-based trigger signal or ankle-based movement strategies for postural balance reactions. These findings are compatible with the hypothesis that stretch-, force- and joint-related proprioceptive receptors at the level of the trunk provide a directionally sensitive triggering mechanism underlying a, minimally, two-stage (pitch-based leg and pitch-and-roll-based trunk) balance-correcting strategy. Accelerometer recordings from the head identified large vertical linear accelerations only for pitch movements and angular roll accelerations only during roll perturbations with latencies as early as 15 ms. Thus, it appears that balance corrections in leg and trunk muscles may receive strong, receptor-dependent (otolith or vertical canal) and directionally sensitive amplitude-modulating input from vestibulospinal signals. Received: 4 September 1998 / Accepted: 30 April 1999     

Triggering of balance corrections and compensatory strategies in a patient with total leg proprioceptive loss

Triggering of balance corrections may depend on both leg and trunk proprioceptive inputs. To study this issue and to determine how a total proprioceptive loss in the legs (ToLPL) would affect postural reactions in different directions, we investigated the postural control of a patient with a long-standing dorsal root ganglionopathy. This patient had absent stretch reflexes at the ankle and knee joints, delayed reflexes at the hips, but normal muscle strength. Postural control was probed with support-surface movements driven by two different experimental protocols. The first protocol concentrated on leg muscle responses by varying ankle inputs during pitch plane perturbations. The second protocol focussed on the directional sensitivity of upper body responses using combined roll and pitch tilt perturbations. For both protocols, identical techniques were used to record ankle torques, angular velocities of the upper legs and trunk, and surface EMG from leg, hip and trunk muscles. For the first protocol, pitch plane stance perturbations with three different ankle inputs were imposed by a movable support surface. A simultaneous 4-cm rearward translation and 4-deg toe-up rotation produced an 80-deg/s "enhanced ankle input", a simple toe-up rotation gave a 40-deg/s "normal" ankle input and a simultaneous 4-cm rearward translation and 4-deg "toe-down" rotation yielding a 0-deg/s "nulled ankle input". Responses in the ToLPL patient were compared to those of healthy controls and those of patients with lower-leg proprioceptive loss (LLPL). Following normal and enhanced ankle input perturbations, stretch reflexes were absent in ankle and knee joint muscles of the ToLPL patient. Balance correcting responses in the lower legs were diminished and delayed by some 45 ms. In quadriceps, balance-correcting responses were larger than normal, peaked earlier and were not delayed. During the nulled ankle input condition, the ankle muscle responses in the ToLPL patient were again diminished and delayed by 40 ms with respect to both normal subjects and LLPL patients. However, the ToLPL patient again generated an earlier, larger, balance correcting response in quadriceps. For the second protocol, combinations of roll and pitch perturbations were also delivered by a moving support surface. The amplitude was 7.5 deg at 50 deg/s. Eight different directions were applied randomly (pure "toes down", pure "toes up" and directions at 45-deg intervals of roll). As with the first protocol pre-stimulus background muscle activity was excessive in all trunk and most leg muscles. Responses to roll tilt produced several striking changes from normal in the ToLPL patient. First reflexes in gluteus medius were delayed. Second, the trunk roll which commences around 30 ms in normals was in the opposite direction. This roll was accompanied by oppositely directed stretch reflexes in paraspinal muscles. Third, directional sensitivity of balance corrections was far more roll oriented in leg and trunk muscles. Fourth, some tilt directions caused a deactivation response of background activity. This "deactivation strategy" strongly contrasted with the strategy of controls who had low pre-stimulus background activity and activated responses around 100 ms to correct postural instability. These findings provide new insights into the generation of pitch and roll plane directed balance corrections based on the interaction of proprioceptive trigger signals from the ankles, knees and hips. Without proprioceptive input from the ankle and knee, ankle muscle responses are delayed but not absent. Upper leg and trunk responses are not delayed. This suggests that most, if not all, lower leg balance correcting responses are triggered by hip and, possibly, trunk proprioceptive inputs. When leg proprioceptive input is absent, balance correcting responses lose pitch plane sensitivity. The solution used by the patient to overcome these deficits was to markedly raise background muscle activity levels, presumably to provide a stiffer body structure. The lack of trunk flexibility and lateral instability this produced for roll tilts was offset by the ability to compensate by using a hitherto not described "deactivation response" strategy. The patient had a clinical picture usually described as "deafferented"; yet our roll tilt perturbations revealed delayed reflex responses in hip muscles. With vestibulospinal and neck-proprioceptive inputs, these responses may have helped with the development of compensation processes for the total leg proprioceptive deficit.     

Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects

One of the signatures of balance deficits observed in vestibular loss subjects is the greater instability in the roll compared to pitch planes. Directional differences in the timing and strengths of vestibular and proprioceptive sensory signals between roll and pitch may lead to a greater miscalculation of roll than pitch motion of the body in space when vestibular input is absent. For this reason, we compared the timing and amplitude of vestibular information, (observable in stimulus-induced head accelerations when subjects are tilted in different directions), with that of proprioceptive information caused by stimulus induced rotations of ankle and hip joints [observable as short latency (SL) stretch responses in leg and trunk muscle EMG activity]. We attempted to link the possible mode of sensory interaction with the deficits in balance control. Six subjects with bilaterally absent vestibular function and 12 age-matched controls were perturbed, while standing, in 8 directions of pitch and roll support surface rotation in random order. Body segment movements were recorded with a motion analysis system, head accelerations with accelerometers, and muscle activity with surface EMG. Information on stimulus pitch motion was available sequentially. Pitch movements of the support surface were best coded in amplitude by ankle rotation velocity, and by head vertical linear acceleration, which started at 13 ms after the onset of ankle rotation. EMG SL reflex responses in soleus with onsets at 46 ms provided a distal proprioceptive correlate to the pitch motion. Roll information on the stimulus was available simultaneously. Hip adduction and lumbo-sacral angular velocity were represented neurally as directionally specific short latency stretch and unloading reflexes in the bilateral gluteus medius muscles and paraspinal muscles with onsets at 28 ms. Roll angular accelerations of the head coded roll amplitude and direction at the same time (31 ms). Significant differences in amplitude coding between vestibular loss subjects and controls were only observed as a weaker coding between stimulus motion and head roll and head lateral linear accelerations. The absence of vestibular inputs in vestibular loss subjects led to characteristic larger trunk in motion in roll in the direction of tilt compared to pitch with respect to controls. This was preceded by less uphill flexion and no downhill extension of the legs in vestibular loss subjects. Downhill arm abduction responses were also greater. These results suggest that in man vestibular inputs provide critical information necessary for the appropriate modulation of roll balance-correcting responses in the form of stabilising knee and arm movements. The simultaneous arrival of roll sensory information in controls may indicate that proprioceptive and vestibular signals can only be interpreted correctly when both are present. Thus, roll proprioceptive information may be interpreted inaccurately in vestibular loss subjects, leading to an incorrect perception of body tilt and insufficient uphill knee flexion, especially as cervico-collic signals appear less reliable in these subjects as an alternative sensory input.     

Spatio-temporal separation of roll and pitch balance-correcting commands in humans

This study was designed to provide evidence for the hypothesis that human balance corrections in response to pitch perturbations are controlled by muscle action mainly about the ankle and knee joints, whereas balance corrections for roll perturbations are controlled predominantly by motion about the hip and lumbro-sacral joints. A dual-axis rotating support surface delivered unexpected random perturbations to the stance of 19 healthy young adults through eight different directions in the pitch and the roll planes and three delays between pitch and roll directions. Roll delays with respect to pitch were no delay, a short 50-ms delay of roll with respect to pitch movements, (chosen to correspond to the onset time of leg muscle stretch reflexes), and a long 150-ms delay between roll and pitch movements (chosen to shift the time when trunk roll velocity peaks to the time when trunk peak pitch velocity normally occurs). Delays of stimulus roll with respect to pitch resulted in delayed roll responses of the legs, trunk, arms, and head consistent with stimulus delay without any changes in roll velocity amplitude. Delayed roll perturbations induced only small changes in the pitch motion of the legs and trunk; however, major changes were seen in the time when roll motion of the trunk was arrested. Amplitudes and directional sensitivity of short-latency (SL) stretch reflexes in ankle muscles were not altered with increasing roll delay. Small changes to balance correcting responses in ankle muscles were observed. SL stretch reflexes in hip and trunk muscles were delayed, and balance-correcting responses in trunk muscles became split into two distinct responses with delayed roll. The first of these responses was small and had a directional responsiveness aligned more along the pitch plane. The main, larger, response occurred with an onset and time-to-peak consistent with the delay in trunk roll displacement and its directional responsiveness was roll oriented. The sum of the amplitudes of these two types of balance-correcting responses remained constant with roll delay. These results support the hypothesis that corrections of the body's pitch and roll motion are programmed separately by neural command signals and provide insights into possible triggering mechanisms. The evidence that lower leg muscle balance-correcting activity is hardly changed by delayed trunk roll also indicates that lower leg muscle activity is not predominant in correcting roll motion of the body. Lower leg and trunk muscle activity appears to have a dual action in balance corrections. In trunk muscles the main action is to correct for roll perturbations and the lesser action may be an anticipatory stabilizing reaction for pitch perturbations. Likewise, the small changes in lower leg muscle activity may result from a generalized stabilizing reaction to roll perturbations, but the main action is to correct for pitch perturbations.     

The effect of voluntary arm abduction on balance recovery following multidirectional stance perturbations

The goal of this study was to investigate how voluntarily abducting one arm, 90° at onset of a rotational perturbation of the support surface, influences the recovery of upright stance. Young adults were tested under four stance conditions: abducting one arm to the horizontal only (AO); perturbation of stance using a support surface rotation only (PO); combined support surface rotation and abduction of the downhill arm, ipsilateral to tilt (IPS); and fourth abduction of the uphill, contralateral arm (CON). Simultaneous auditory and visual trigger cues were used for arm raising. Perturbations consisted of six directions of combined support surface roll and pitch rotation (7.5° and 60°/s). Outcome measures were whole body centre of mass (COM) movements and body segment angular displacements recorded with a motion analysis system, as well as leg, trunk, and arm EMG responses. Arm raises contralateral and ipsilateral to the direction of support surface roll were more rapid than in the AO condition and significantly reduced or increased, respectively, COM lateral displacements relative to the PO condition. The changes in COM displacements and velocities during combined CON arm raise and perturbation were greater than expected from the sum of displacements for AO and PO conditions alone, but less for the IPS condition. Arm raising increased trunk roll in a direction opposite arm raising was more than for the AO and PO conditions. Robust effects were also observed for hip abduction but not for leg flexion. Early balance correcting activity was enhanced on the side opposite arm raising and later stabilising activity reduced bilaterally in lower trunk muscles compared to summed activity for the AO and PO conditions. Similar effects were observed in gluteus medius muscles but effects were weak in ankle muscles. EMG onsets in muscles of the raised arm were earlier than in the AO conditions. We conclude that triggered arm abduction, contralateral to the direction of support surface rotation, had significant stabilization benefits for young adults and ipsilateral arm movements had destabilizing effects. The arm raises could be simultaneously executed with balance corrections. These results provide insights into the integration of balance corrections and voluntary commands into one automatic reaction that may be useful in training fall avoidance.     

Balance control in patients with distal versus proximal muscle weakness

Muscle weakness is consistently associated with falls in the elderly people, typically when present along with other risk factors. However, it remains unknown whether and how muscle weakness alone affects balance. This hampers development of more effective fall prevention strategies. Clinical observations suggest that the amount and distribution of muscle weakness influences balance control. We therefore investigated balance corrections in patients with either predominantly proximal (limb girdle muscular dystrophy (LGMD); n=8) or distal (distal spinal muscular atrophy; n=5) leg weakness, and 27 matched healthy controls. Balance was perturbed using surface tilt rotations that were delivered randomly in eight directions. Balance measures were full body kinematics and surface electromyographic activity (EMG) of leg, arm, and trunk muscles. Both patient groups were more unstable than controls, as reflected by greater excursions of the centre of mass (COM), especially in the pitch (anterior–posterior (AP)) plane. COM displacements were greater in distal weakness patients. Patients with distal weakness had excessive and unstable trunk, knee and ankle movements, and this was present following both forward and backward directed balance perturbations, possibly reflecting the greater use of distal leg muscles in these directions. In contrast, the less weak proximal weakness patients demonstrated unstable trunk and ankle movements only for backward directed balance perturbations. Both patient groups used arm movements to compensate for their instability. We conclude that primarily distal but also proximal muscle weakness leads to significant postural instability. This observation, together with the retained ability of patients to use compensatory arm movements, provides targets that may be amenable to improvement with therapeutic intervention.     

Incorporating voluntary unilateral knee flexion into balance corrections elicited by multi-directional perturbations to stance

Positive effects on lateral center of mass (CoM) shifts during balance recovery have been seen with voluntarily unilateral arm raising but not with voluntarily bilateral knee flexion. To determine whether unilateral voluntary knee movements can be effectively incorporated into balance corrections we perturbed the balance of 30 young healthy subjects using multi-directional rotations of the support surface while they simultaneously executed unilateral knee flexion. Combined pitch and roll rotations (7.5° and 60°/s) were presented randomly in six different directions. Subjects were tested in four stance conditions: balance perturbation only (PO); cued flexion of one knee only (KO); combined support surface rotation and cued (at rotation onset) flexion of the uphill knee, contralateral to tilt (CONT), or of the downhill knee, ipsilateral to tilt (IPS). Outcome measures were CoM motion and biomechanical and electromyography (EMG) responses of the legs, arms and trunk. Predicted measures (PO+KO) were compared with combined measures (CONT or IPS). Unilateral knee flexion of the uphill knee (CONT) provided considerable benefit in balance recovery. Subjects rotated their pelvis more to the uphill side than predicted. Downhill knee bending (IPS) also had a positive effect on CoM motion because of a greater than predicted simultaneous lateral shift of the pelvis uphill. KO leg muscle activity showed anticipatory postural activity (APA) with similar profiles to early balance correcting responses. Onsets of muscle responses and knee velocities were earlier for PO, CONT, and IPS compared to KO conditions. EMG response amplitudes for CONT and IPS conditions were generally not different from the PO condition and therefore smaller than predicted. Later stabilizing responses at 400 ms had activation amplitudes generally equal to those predicted from the PO+KO conditions. Our results suggest that because EMG patterns of anticipatory postural activity of voluntary unilateral knee flexion and early balance corrections have similar profiles, the CNS is easily able to incorporate voluntary activation associated with unilateral knee flexion into automatic postural responses. Furthermore, the effect on movement strategies appears to be non-linear. These findings may have important implications for the rehabilitation of balance deficits.     

Influence of postural anxiety on postural reactions to multi-directional surface rotations

Previous studies have shown significant effects of increased postural anxiety in healthy young individuals when standing quietly or performing voluntary postural tasks. However, little is known about the influence of anxiety on reactive postural control. The present study examined how increased postural anxiety influenced postural reactions to unexpected surface rotations in multiple directions. Ten healthy young adults (mean age: 25.5 yr, range: 22-27 yr) were required to recover from unexpected rotations of the support surface (7.5 degrees amplitude, 50 degrees/s velocity) delivered in six different directions while standing in a low postural threat (surface height: 60 cm above ground) or high postural threat (surface height: 160 cm above ground) condition. Electromyographic data from 12 different postural leg, hip, and trunk muscles was collected simultaneously. Full body kinematic data were also used to determine total body center of mass (COM) and segment displacements. Four distinct changes were observed with increased postural anxiety: increased amplitude in balance-correcting responses (120-220 ms) in all leg, trunk, and arm muscles; decreased onset latency of deltoid responses; reduced magnitude of COM displacement; and reduced angular displacement of leg, pelvis, and trunk. These observations suggest that changes in dynamic postural responses with increased anxiety are mediated by alterations in neuro-muscular control mechanisms and thus may contribute significantly to the pathophysiology of balance deficits associated with aging or neurological disease.     

The influence of artificially increased hip and trunk stiffness on balance control in man

Lightweight corsets were used to produce mid-body stiffening, rendering the hip and trunk joints practically inflexible. To examine the effect of this artificially increased stiffness on balance control, we perturbed the upright stance of young subjects (20–34 years of age) while they wore one of two types of corset or no corset at all. One type, the half-corset, only increased hip stiffness, and the other, the full-corset, increased stiffness of the hips and trunk. The perturbations consisted of combined roll and pitch rotations of the support surface (7.5 deg, 60 deg/s) in one of six different directions. Outcome measures were biomechanical responses of the legs, trunk, arms and head, and electromyographic (EMG) responses from leg, trunk, and upper arm muscles. With the full-corset, a decrease in forward stabilising trunk pitch rotation compared to the no-corset condition occurred for backward pitch tilts of the support surface. In contrast, the half-corset condition yielded increased forward trunk motion. Trunk backward pitch motion after forwards support-surface perturbations was the same for all corset conditions. Ankle torques and lower leg angle changes in the pitch direction were decreased for both corset conditions for forward pitch tilts of the support-surface but unaltered for backward tilts. Changes in trunk roll motion with increased stiffness were profound. After onset of a roll support-surface perturbation, the trunk rolled in the opposite direction to the support-surface tilt for the no-corset and half-corset conditions, but in the same direction as the tilt for the full-corset condition. Initial head roll angular accelerations (at 100 ms) were larger for the full-corset condition but in the same direction (opposite platform tilt) for all conditions. Arm roll movements were initially in the same direction as trunk movements, and were followed by large compensatory arm movements only for the full-corset condition. Leg muscle (soleus, peroneus longus, but not tibialis anterior) balance-correcting responses were reduced for roll and pitch tilts under both corset conditions. Responses in paraspinals were also reduced. These results indicate that young healthy normals cannot rapidly modify movement strategies sufficiently to account for changes in link flexibility following increases in hip and trunk stiffness. The changes in leg and trunk muscle responses failed to achieve a normal roll or pitch trunk end position at 700 ms (except for forward tilt rotations), even though head accelerations and trunk joint proprioception seemed to provide information on changed trunk movement profiles over the first 300 ms following the perturbation. The major adaptation to stiffness involved increased use of arm movements to regain stability. The major differences in trunk motion for the no-corset, half-corset and full-corset conditions support the concept of a multi-link pendulum with different control dynamics in the pitch and roll planes as a model of human stance. Stiffening of the hip and trunk increases the likelihood of a loss of balance laterally and/or backwards. Thus, these results may have implications for the elderly and others, with and without disease states, who stiffen for a variety of reasons.     

Spatial coordination by descending vestibular signals

Electromyographic activity of dorsal neck muscles and neck torques was recorded to study vestibulocollic, cervicocollic, and combined reflexes in alert and decerebrate cats during rotations of the whole body, the body except for the head, and the head but not the rest of the body. Cats were rotated about many axes that lay in the frontal, sagittal, and horizontal planes using sinusoidal 0.25-Hz waveforms or sum-of-sinusoid waveforms. Robust electromyographic responses were recorded from six muscles, with response directionality that in most cases did not show strong dependence on the reflex tested or on other factors including exact neck angle, stimulus amplitude from 5° to 60°, and intact versus decerebrate state. Based on the strength of responses to rotations about all the tested axes, neck muscles could be characterized by maximal activation direction vectors representing the axis and direction of rotation in threedimensional space that was most excitatory during reflex responses. Responses to rotations about axes that lay in a coordinate plane were predicted by a cosine function of the angle between the axis under test and the maximally excitatory axis in the plane. All muscles were excited by the nose down phase of pitch rotation and by yaw and roll away from the side on which the muscle lay. Biventer cervicis was best activated by rotations with axes near nose-down pitch, and its axis of maximal activation also had small, approximately equal components of yaw and roll toward the contralateral side. Complexus was best excited by rotations with axes nearest roll, but with large components along all three axes. Occipitoscapularis was best excited by rotations about axes near pitch, but with a moderately large contralateral yaw component and a smaller but significant contralateral roll component. Splenius was best excited by rotations with a large component of contralateral yaw, considerable nose-down pitch, and a smaller component of contralateral roll. Rectus major was best excited by rotations near nose-down pitch, but with a substantial contralateral yaw component and smaller contralateral roll component. Obliquus inferior was best excited by rotations with a large component of contralateral yaw, but with considerable contralateral roll and nose-down pitch components. All muscles responded as though they received convergent input from all three semicircular canals. Vestibulocollic and combined reflex responses in alert cats and vestibulocollic, cervicocollic, and combined responses in decerebrate cats appeared to have the same directionality, as evidenced by insignificant shifts in maximal activation vectors. Cervicocollic responses in alert cats were inconsistent and often absent, but appeared upon decerebration, suggesting that higher centers suppress the cervicocollic reflex in intact animals. Decerebration and partial cerebellectomy had no significant effect on maximal activation directions, although electromyographic response magnitudes increased after each. The results suggest that common circuits or strategies are used by neck stretch and vestibular-neck reflexes. The reflex excitation directions do not match the mechanical actions of the neck muscles but agree fairly well with previously published predictions of a mathematical model of neck motor control.     

Electromyographic activity of dorsal neck muscles in squirrel monkeys during rotations in an upright or upside down posture

Electromyographic (EMG) activity was recorded from occipitoscapularis, semispinalis, and splenius neck muscles in five alert squirrel monkeys during 0.25-Hz rotations about horizontal axes oriented at 22.5 degrees intervals, including pitch, roll, and intermediate axes. The animals were oriented in either upright or upside down posture. In the upright posture, all monkeys exhibited compensatory EMG activity with maximal activation during rotations about axes between pitch in the pitch forward direction and contralaterally directed roll. Response timing varied across animals with EMG peaks ranging from near pitch forward head velocity to near pitch forward head position. When the head was upside down, response dynamics and directionality were altered to varying degrees in different monkeys. The greatest change in response to head inversion was seen in the monkey that had response phases closest to head position, the least in the animal with phases closest to head velocity. The monkey with EMG response peaks closest to position phase showed nearly 180 degrees inversion of responses when the head was upside down, suggesting that in this monkey a righting reflex mediated by utricular signals was activated in the upside down posture. The monkey with EMG response peaks closest to velocity phase may have lacked a righting response and exhibited only a canal-mediated compensatory vestibulocervical reflex in both upright and upside down postures. The results suggest that reflex contraction of neck muscles in response to passive head rotation includes an interplay of compensatory and righting responses that varies from animal to animal.     

Interactions between vestibular and proprioceptive inputs triggering and modulating human balance-correcting responses differ across muscles

Interactions between proprioceptive and vestibular inputs contributing to the generation of balance corrections may vary across muscles depending on the availability of sensory information at centres initiating and modulating muscle synergies, and the efficacy with which the muscle action can prevent a fall. Information which is not available from one sensory system may be obtained by switching to another. Alternatively, interactions between sensory systems and the muscle to which this interaction is targeted may be fixed during neural development and not switchable. To investigate these different concepts, balance corrections with three different sets of proprioceptive trigger signals were examined under eyes-open and eyes-closed conditions in the muscles of normal subjects and compared with those of subjects with bilateral peripheral vestibular loss. The different sets of early proprioceptive inputs were obtained by employing three combinations of support surface rotation and translation, for which ankle inputs were nulled, normal or enhanced, the knees were either locked or in flexion, and the trunk was either in flexion or extension. Three types of proprioceptive and vestibulospinal interactions were identified in muscles responses. These interactions were typified by the responses of triceps surae, quadriceps, and paraspinal muscles. The amplitudes of stretch responses at 50 ms after the onset of ankle flexion in triceps surae muscles were related to the velocity of ankle stretch. The amplitude of balance-correcting responses at 100 ms corresponded more with stretch of the biarticular gastrocnemius when the knee was re-extended at 60 ms. Absent stretch reflexes at 50 ms in triceps surae with nulled ankle inputs caused a minor, 12-ms delay in the onset of balance-correcting responses in triceps surae muscles. Vestibular loss caused no change in the amplitude of balance-correcting responses, but a negligible decrease in onset latency in triceps surae even with nulled ankle inputs. Stretch responses in quadriceps at 80 ms increased with the velocity of knee flexion but were overall lower in amplitude in vestibular loss subjects. Balance-correcting responses in quadriceps had amplitudes which were related to the directions of initial trunk movements, were still present when knee inputs were negligible and were also altered after vestibular loss. Stretch and unloading responses in paraspinals at 80 ms were consistent with the direction of initial trunk flexion and extension. Subsequent balance-correcting responses in paraspinals were delayed 20 ms in onset and altered in amplitude by vestibular loss. The changes in the amplitudes of ankle (tibialis anterior), knee (quadriceps) and trunk (paraspinal) muscle responses with vestibular loss affected the amplitudes and timing of trunk angular velocities, requiring increased stabilizing tibialis anterior, paraspinal and trapezius responses post 240 ms as these subjects attempted to remain upright. The results suggest that trunk inputs provide an ideal candidate for triggering balance corrections as these would still be present when vestibular, ankle and knee inputs are absent. The disparity between the amplitudes of stretch reflex and automatic balance-correcting responses in triceps surae and the insignificant alteration in the timing of balance-correcting responses in these muscles with nulled ankle inputs indicates that ankle inputs do not trigger balance corrections. Furthermore, modulation of balance corrections normally performed by vestibular inputs in some but not all muscles is not achieved by switching to another sensory system on vestibular loss. We postulate that a confluence of trunk and upper-leg proprioceptive input establishes the basic timing of automatic, triggered balance corrections which is then preferentially weighted by vestibular modulation in muscles that prevent falling. The organisation of balance corrections around trunk inputs portrayed here would have considerable advantage for the infant learning balance control, but forces balance control centres to rely on limited sensory information related to this most unstable body segment, the trunk, when triggering balance corrections. Received: 13 October 1997 / Accepted: 30 March 1998     

Incorporating voluntary knee flexion into nonanticipatory balance corrections

Knee movements play a critical role in most balance corrections. Loss of knee flexibility may cause postural instability. Conversely, trained voluntary knee flexions executed during balance corrections might help to overcome balance deficits. We examined whether bilateral knee flexion could be added to automatic balance corrections generated by sudden balance perturbations. We investigated how this could be achieved and whether it improved or worsened balance control. Twenty-four healthy subjects participated in three different test conditions, in which they had to flex their knees following an auditory cue (VOLUNTARY condition), had to restore their balance in response to multidirectional rotations of a support surface (REACTIVE condition), or the combination of these two (COMBINED condition). A new variable set (PREDICTED), calculated as the mathematical sum of VOLUNTARY and REACTIVE, was compared with the COMBINED variable set. COMBINED responses following forward rotations were close to PREDICTED, or greater, suggesting adequate integration of knee flexion into the automatic balance reactions. For backward rotations, the COMBINED condition resulted in several near-falls, and this was generally associated with smaller knee flexion and smaller EMG responses. Subjects compensated by using greater trunk flexion and arm movements. Activity in several muscles displayed earlier onsets for the COMBINED condition following backward rotations. We conclude that healthy adults can incorporate voluntary knee flexion into their automatic balance corrections and that this depends on the direction of the postural perturbation. These findings highlight the flexibility of the human balance repertoire and underscore both the advantages and limitations of using trained voluntary movements to aid balance corrections in man.     

Multi-digit control of contact forces during rotation of a hand-held object

Rotation of an object held with three fingers is produced by modulation of force amplitude and direction at one or more contact points. Changes in the moment arm through which these forces act can also contribute to the modulation of the rotational moment. Therefore force amplitude and direction as well as the center of pressure on each contact surface must be carefully coordinated to produce a rotation. Because there is not a single solution, this study sought to describe consistent strategies for simple position-to-position rotations in the pitch, roll, and yaw axes. Force amplitude and direction, and center of pressure on the contact surfaces (and thus the moment arm), were measured as human subjects rotated a 420 g force-transducer instrumented object, grasped with the thumb, index and ring fingers (average movement time: 500 ms). Electromyographic (EMG) activity was recorded from five intrinsic and three extrinsic hand muscles and two wrist muscles. Principal components analysis of force and EMG revealed just two main temporal patterns: the main one followed rotational position and the secondary one had a time course that resembled that of rotational velocity. Although the task could have been accomplished by dynamic modulation of the activity of wrist muscles alone, these two main dynamic EMG patterns were seen in intrinsic hand muscles as well. In contrast to previous reports of shifting in time of the phasic activity bursts of various muscles, in this task, all EMG records were well described by just two temporal patterns, resembling the position and velocity traces.     

Dynamics and directionality of the vestibulo-collic reflex (VCR) in mice

The vestibulo-collic reflex (VCR) stabilizes the head in space by excitation of neck muscles that oppose head rotation. Recently, the mouse vestibulo-ocular reflex (VOR) has been characterized so that genetic manipulations of the vestibular system can be examined. We have characterized the dynamics and directionality of the VCR in mice restrained at the neck so that studies of vestibular system genetics may include comparisons to normal VCR in addition to VOR. Head rotations were measured in darkness with a three-dimensional search coil system during whole body rotations. The VCR in four C57BL/6 mice was present in pitch, roll, and yaw directions with an overall average gain of 0.28. Phase was accurately compensatory to oppose head rotation across a wide range of frequencies from 0.02 Hz to 2.0 Hz. Compensatory head rotations were greatest in the direction opposing the applied stimulus and weak or absent in other directions. Constant velocity rotations about horizontal axes elicited head velocity modulation and bias similar to that observed in the VOR. We conclude that the VCR of mice is similar to that in other mammals.     

Modulation of phasic and tonic muscle synergies with reaching direction and speed

How the CNS masters the many degrees of freedom of the musculoskeletal system to control goal-directed movements is a long-standing question. We have recently provided support to the hypothesis that the CNS relies on a modular control architecture by showing that the phasic muscle patterns for fast reaching movements in different directions are generated by combinations of a few time-varying muscle synergies: coordinated recruitment of groups of muscles with specific activation profiles. However, natural reaching movements occur at different speeds and require the control of both movement and posture. Thus we have investigated whether muscle synergies also underlie reaching at different speeds as well as the maintenance of stable arm postures. Hand kinematics and shoulder and elbow muscle surface EMGs were recorded in five subjects during reaches to eight targets in the frontal plane at different speeds. We found that the amplitude modulation of three time-invariant synergies captured the variations in the postural muscle patterns at the end of the movement. During movement, three phasic and three tonic time-varying synergies could reconstruct the time-normalized muscle pattern in all conditions. Phasic synergies were modulated in both amplitude and timing by direction and speed. Tonic synergies were modulated only in amplitude by direction. The directional tuning of both types of synergies was well described by a single or a double cosine function. These results suggest that muscle synergies are basic control modules that allow generating the appropriate muscle patterns through simple modulation and combination rules.     

Adapting locomotion to different surface compliances: neuromuscular responses and changes in movement dynamics

Knowledge of how the nervous system deals with surfaces with different physical properties such as compliance that challenge balance during locomotion is of importance as we are constantly faced with these situations every day. The purpose of this study was to examine the control of center of mass (COM) and lower limb dynamics and recovery response modulation of muscle activity during locomotion across an unexpected compliant surface and in particular, scaling behavior across different levels of compliance. Eight young adults walked along a walkway and stepped on an unexpected compliant surface in the middle of the travel path. There were three different levels of surface compliance, and participants experienced either no compliant surface or one of the three compliant surfaces during each trial that were presented in a blocked or random fashion. Whole body kinematics were collected along with surface electromyography (EMG) of selected bilateral lower limb and trunk muscles. The recovery response to the first compliant-surface trial demonstrated muscle onset latencies between 97 and 175 ms, and activity was modulated while on the compliant surface. Vertical COM trajectory was not preserved after contact with the compliant surface: peak vertical COM, while on the compliant surface was lower than when on stable ground. Perturbed-limb knee flexion after toe-off increased with increased surface compliance, which enabled toe clearance with the ground to be similar to control trials. The results suggest that stepping off of a compliant surface is actively modulated by the CNS and is geared toward maintaining dynamic stability.