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     

Differential control of abdominal muscles during multi-directional support-surface translations in man

The current study aimed to understand how deep and superficial abdominal muscles are coordinated with respect to activation onset times and amplitudes in response to unpredictable support-surface translations delivered in multiple directions. Electromyographic (EMG) data were recorded intra-muscularly using fine-wire electrodes inserted into the right rectus abdominis (RA), obliquus externus (OE), obliquus internus (OI) and transversus abdominis (TrA) muscles. Twelve young healthy male subjects were instructed to maintain their standing balance during 40 support surface translations (peak acceleration 1.3 m s⁻²; total displacement 0.6 m) that were counter-balanced between four different directions (forward, backward, leftward, rightward). Differences between abdominal muscles in EMG onset times were found for specific translation directions. The more superficial RA (backward translations) and OE (forward and leftward translations) muscles had significantly earlier EMG onsets compared to TrA. EMG onset latencies were dependent on translation direction in RA, OE and OI, but independent of direction in TrA. EMG amplitudes in RA and OE were dependent on translation direction within the first 100 ms of activity, whereas responses from the two deeper muscles (TrA and OI) were independent of translation direction during this interval. The current results provide new insights into how abdominal muscles contribute to postural reactions during human stance. Response patterns of deep and superficial abdominal muscles during support surface translations are unlike those previously described during upper-body perturbations or voluntary arm movements, indicating that the neural mechanisms controlling individual abdominal muscles are task-specific to different postural demands.     

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     

Control of reactive balance adjustments in perturbed human walking: roles of proximal and distal postural muscle activity

Studies on the proactive control of gait have shown that proximal (hip/trunk) muscles are the primary contributors to balance control, while studies on reactive balance control during perturbed gait, examining only activity in distal (leg/thigh) muscles, have shown that these muscles are important in compensating for a gait disturbance. This study tested the hypothesis that proximal muscles are also primary contributors to reactive balance control during perturbed gait. Thirty-three young adults participated in a study in which an anterior slip was simulated at heel strike by the forward displacement of a force plate on which they walked. Surface electromyographic data were recorded from bilateral leg, thigh, hip and trunk muscles. Kinematic data were collected on joint angle changes in response to the perturbation. The results did not support the hypothesis that the proximal muscles contribute significantly to balance control during perturbed gait. The proximal muscles did not demonstrate more consistent activation, earlier onset latency, longer burst duration or larger burst magnitude than distal muscles. Moreover, although proximal postural activity was often present in the first slip trial, it tended to adapt away in later trials. By contrast, the typical postural responses exhibited by young adults consisted of an early (90–140 ms), high-magnitude (4–9 times muscle activity during normal walking) and relatively long duration (70–200 ms) activation of bilateral anterior leg muscles as well as the anterior and posterior thigh muscles. Thus, postural activity from bilateral leg and thigh muscles and the coordination between the two lower extremities were the key to reactive balance control and were sufficient for regaining balance within one gait cycle. The adaptive attenuation of proximal postural activity over repeated trials suggests that the nervous system overcompensates for a novel balance threat in the first slip trial and fine-tunes its responses with experience. Received: 24 March 1997 /Accepted: 4 September 1997     

The effect of aging on anticipatory postural control

The aim of the study was to investigate the differences in anticipatory postural adjustments (APAs) between young and older adults and its effect on subsequent control of posture. Ten healthy older adults and thirteen healthy young adults were exposed to predictable external perturbations using the pendulum impact paradigm. Electromyographic activity of the trunk and leg muscles, the center of pressure (COP), and center of mass (COM) displacements in the anterior–posterior direction were recorded and analyzed during the anticipatory and compensatory postural adjustments (CPAs) phases of postural control. The effect of aging was seen as delayed anticipatory muscle activity and larger compensatory muscle responses in older adults as compared to young adults. Moreover, in spite of such larger reactive responses, older adults were still more unstable, exhibiting larger COP and COM peak displacements after the perturbation than young adults when exposed to similar postural disturbances. Nonetheless, while APAs are impaired in older adults, the ability to recruit muscles anticipatorily is largely preserved; however, due to their smaller magnitudes and delayed onsets, it is likely that their effectiveness in reducing the magnitude of CPAs is smaller. The outcome of the study lends support toward investigating the ways of improving anticipatory postural control in people with balance impairments due to aging or neurological disorders.     

Comparison of external load compensation during rhythmic arm movements and rhythmic jaw movements in humans.

Experiments were performed on human elbow flexor and extensor muscles and jaw-opening and -closing muscles to observe the effect on rhythmic movements of sudden loading. The load was provided by an electromagnetic device, which simulated the appearance of a smoothly increasing spring-like load. The responses to this loading were compared in jaw and elbow movements and between expected and unexpected disturbances. All muscles showed electromyographic responses to unexpected perturbations, with latencies of approximately 65 ms in the arm muscles and 25 ms in the jaw. When loading was predictable, anticipatory responses started in arm muscles approximately 200 ms before and in jaw muscles 100 ms before the onset of loading. The reflex responses relative to the anticipatory responses were smaller for the arm muscles than for the jaw muscles. The reflex responses in the arm muscles were the same with unexpected and expected perturbations, whereas anticipation increased the reflex responses in the jaw muscles. Biceps brachii and triceps brachii showed similar sensory-induced responses and similar anticipatory responses. Jaw muscles differed, however, in that the reflex response was stronger in masseter than in digastric. It was concluded that reflex responses in the arm muscles cannot overcome the loading of the arm adequately, which is compensated by a large centrally programmed response when loading is predictable. The jaw muscles, particularly the jaw-closing muscles, tend to respond mainly through reflex loops, even when loading of the jaw is anticipated. The differences between the responses of the arm and the jaw muscles may be related to physical differences. For example, the jaw was decelerated more strongly by the load than the heavier arm. The jaw was decelerated strongly but briefly, <30 ms during jaw closing, indicating that muscle force increased before the onset of reflex activity. Apparently, the force-velocity properties of the jaw muscles have a stabilizing effect on the jaw and have this effect before sensory induced responses occur. The symmetrical responses in biceps and triceps indicate similar motor control of both arm muscles. The differences in reflex activity between masseter and digastric muscle indicate fundamental differences in sensory feedback to the jaw-closing muscle and jaw-opening muscle.     

Anticipatory postural muscle activity associated with bilateral arm flexion while standing in individuals with spastic diplegic cerebral palsy: A pilot study

Compared to automatic postural responses to external perturbation, little is known about anticipatory postural adjustments in individuals with spastic diplegic cerebral palsy. In this study, we examined whether anticipatory activation of postural muscles would be observed before voluntary arm movement while standing in individuals with spastic diplegia. Seven individuals with spastic diplegia (SDCP_group, 12–22 years) and 7 age- and gender-matched individuals without disability (Control_group) participated in this study. Participants performed bilateral arm flexion at maximum speed at their own timing while standing, during which electromyographic (EMG) activities of focal and postural muscles were recorded. In both groups, the erector spinae (ES) and medial hamstring (MH) muscles were activated in advance of the anterior deltoid muscle (AD), which is a focal muscle of arm flexion. Although start times of ES and MH with respect to AD were similar in the 2 groups, increases in EMG amplitudes of ES and MH in the anticipatory range from −150 ms to +50 ms, with respect to burst onset of AD, were significantly smaller in the SDCP_group than in the Control_group. These findings suggest that individuals with spastic diplegia have the ability to anticipate the effects of disturbance of posture and equilibrium caused by arm movement and to activate postural muscles in advance of focal muscles. However, it is likely that the anticipatory increase in postural muscle activity is insufficient in individuals with spastic diplegia.     

Postural adjustments accompanying fast pointing movements in standing, sitting and lying adults

The present study evaluated the effect of different positions, which varied in the amount of bodily support, on postural control during fast pointing movements. Fourteen adult subjects were studied in standing, various sitting and lying positions. Multiple surface electromyograms (EMGs) of arm, neck, trunk and upper leg muscles and kinematics were recorded during a standard series of unilateral arm movements. Two additional series, consisting of bilateral arm movements and unilateral arm movements with an additional weight, were performed to assess whether additional task-load affected postural adjustments differently in a sitting and standing position. Two pointing strategies were used – despite identical instructions. Seven subjects showed an elbow extension throughout the movements. They used the deltoid (DE) as the prime mover (DE group). The other seven subjects performed the movement with a slight elbow flexion and used the biceps brachii (BB) as the prime mover (BB group). The two strategies had a differential effect on the postural adjustments: postural activity was less and substantially later in the BB-group than in the DE group. Anticipatory postural muscle activity was only present in the DE group during stance. In all positions and task-load conditions the dorsal postural muscles were activated before their ventral antagonists. The activation rate, the timing and – to a lesser extent – the amplitude of the dorsal muscle activity was position dependent. The position dependency was mainly found in the caudally located lumbar extensor (LE) and hamstrings (HAM) muscles. The EMG amplitude of LE and HAM was also affected by body geometry (trunk and pelvis position). Position and body geometry had only a minor effect on the activity of the neck and thoracic extensor muscles. This difference in behaviour of lower and upper postural muscles suggests that they could serve different postural tasks: the lower muscles being more involved in keeping the centre of mass within the limits of the support surface, and the upper ones in counteracting the reaction forces generated by movement onset. Increasing task-load by performing bilateral movements and – to a minor extent – during loaded unilateral movements affected the temporal and quantitative characteristics of the postural adjustments during standing and sitting in a similar way. The effect was present mainly during the early part of the response (within 100 ms after prime mover onset). This suggests that feedforward or anticipatory mechanisms play a major role in the task-specific modulation of postural adjustments. Received: 9 April 1997 / Accepted: 9 October 1997     

Automatic postural responses in the cat: Responses to headward and tailward translation

EMG responses, vertical and A-P shear forces and kinematics of "automatic postural responses" to unexpected translational perturbations in the headward and tailward directions were studied in cats. Muscles acting on the major joints of the forelimbs and hindlimbs were studied. Movement of the animals in response to perturbation were highly stereotyped and consisted of two phases: (1) motion of the feet during platform movement while the trunk remained relatively stationary followed by (2) active correction of posture by movement of the trunk in the direction of perturbation. Vertical force changes occurred after the perturbation was well underway (latency 65 ms) and were related to the displacement of the center of mass and active correction of trunk position. Shear forces showed both passive (inertial) and active components and suggested that the majority of the torque necessary for postural correction was generated by the hindlimb. EMG responses in forelimb and shoulder muscles were most correlated with increase in vertical force, showing a generalized co-contraction in tailward translation (when these limbs were loaded) and little activity when the forelimbs were unloaded. EMG responses in hindlimb showed reciprocal activation of agonists and antagonists during perturbation with strong synergies of thigh and foot flexors in tailward translation and thigh and foot extensors in headward translation. The forelimb EMG patterns were most consistent with the conclusion that the forelimb is used primarily for vertical support during perturbation. It was concluded that hindlimb EMG responses were appropriate for both vertical support and performance of the postural correction. The hindlimb muscle synergies observed during translation are the "mirror image" of those observed in humans by other workers.     

Effect of lower limb muscle fatigue on anticipatory postural adjustments associated with bilateral-forward reach in the unipedal dominant and non-dominant stance

Voluntary arm movements are preceded by dynamical and electromyographical (EMG) phenomena in “postural segments” (i.e. body segments not directly involved in the voluntary movement) called “anticipatory postural adjustments” (APA). The present study examined how the central nervous system organizes APA under fatigued state of postural musculature elicited by series of high-level isometric contractions (HIC), i.e. corresponding to 60% of maximal voluntary contraction. Subjects (N = 14) purposely performed series of bilateral-forward reach task (BFR) under unipodal stance (dominant and non-dominant) before (“no fatigue” condition, NF) and after (“fatigue” condition, F) a procedure designed to obtain major fatigue in hamstrings. Centre-of-gravity acceleration, centre-of-pressure displacement, and electrical activity of trunk and leg muscles were recorded and quantified within a time-window typical of APA. Results showed that there was no significant effect of fatigue on the level of muscle excitation and APA onset in any of the postural muscles recorded. Similarly, no change in APA onset could be detected from the biomechanical traces. In contrast, results showed that the amplitude of anticipatory centre-of-pressure displacement and centre-of-gravity acceleration reached lower value in F than in NF. Similar results were obtained whether dominant or non-dominant leg was considered. The changes in biomechanical APA features could not be ascribed to a different focal movement performance (maximal BFR velocity and acceleration) between F and NF. These results suggest that, when fatigue is induced by HIC, the capacity of the central nervous system to adapt APA programming to the fatigued state of the postural muscle system might be altered.     

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.     

Time-based prediction in motor control: evidence from grip force response to external load perturbations

An object held in precision grip creates predictable load forces on the hand during voluntary hand movement and these are associated with anticipatory modulation of grip force. Conflicting results have been obtained over whether predictable external load perturbations result in anticipatory grip force responses (e.g. Blakemore et al. in J Neurosci 18(18):7511–7518, 1998; Weeks et al. in Exp Brain Res 132:404–410, 2000). This paper investigated whether the discrepancies reflect differences in the methods used in estimating the time delay. Subjects held a manipulandum that delivered load force perturbations in the form of pulses of variable duration and interval or periodic 0.5 and 1 Hz square waves or sinusoids. The grip forces exerted by the subjects were measured. Two methods were used to assess the time delay of the grip force in relation to the load force: (1) cross-spectral analysis, (2) a single threshold method applied on time-locked averaged data. Despite a phase lag shown by the cross-spectral analysis, the threshold method revealed grip force increased 264.8±40.2 ms before the onset of the load force when 0.5 Hz square waves were used as the load force perturbation and 70.2±17.0 ms before the load force when 1 Hz square waves were used. Computer simulations indicated that the single threshold method gives a more sensitive estimate of the onset time than the cross-spectral analysis. We conclude that discrepancies in previous studies reflect differences in the methods used to assess the time-delay and that there is an anticipatory component in the grip force response to predictable external load perturbation.     

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.     

Vertical perturbations of human gait: organisation and adaptation of leg muscle responses

During the last several years, evidence has arisen that the neuronal control of human locomotion depends on feedback from load receptors. The aim of the present study was to determine the effects and the course of sudden and unexpected changes in body load (vertical perturbations) on leg muscle activity patterns during walking on a treadmill. Twenty-two healthy subjects walking with 25% body weight support (BWS) were repetitively and randomly loaded to 5% or unloaded to 45% BWS during left mid-stance. At the new level of BWS, the subjects performed 3–11 steps before returning to 25% BWS (base level). EMG activity of upper and lower leg muscles was recorded from both sides. The bilateral leg muscle activity pattern changed following perturbations in the lower leg muscles and the net effect of the vertical perturbations showed onset latencies with a range of 90–105 ms. Body loading enhanced while unloading diminished the magnitude of ipsilateral extensor EMG amplitude, compared to walking at base level. Contralateral leg flexor burst activity was shortened following loading and prolonged following unloading perturbation while flexor EMG amplitude was unchanged. A general decrease in EMG amplitudes occurred during the course of the experiment. This is assumed to be due to adaptation. Only the muscles directly activated by the perturbations did not significantly change EMG amplitude. This is assumed to be due to the required compensation of the perturbations by polysynaptic spinal reflexes released following the perturbations. The findings underline the importance of load receptor input for the control of locomotion.     

A history of low back pain associates with altered electromyographic activation patterns in response to perturbations of standing balance

People with a history of low back pain (LBP) exhibit altered responses to postural perturbations, and the central neural control underlying these changes in postural responses remains unclear. To characterize more thoroughly the change in muscle activation patterns of people with LBP in response to a perturbation of standing balance, and to gain insight into the influence of early- vs. late-phase postural responses (differentiated by estimates of voluntary reaction times), this study evaluated the intermuscular patterns of electromyographic (EMG) activations from 24 people with and 21 people without a history of chronic, recurrent LBP in response to 12 directions of support surface translations. Two-factor general linear models examined differences between the 2 subject groups and 12 recorded muscles of the trunk and lower leg in the percentage of trials with bursts of EMG activation as well as the amplitudes of integrated EMG activation for each perturbation direction. The subjects with LBP exhibited 1) higher baseline EMG amplitudes of the erector spinae muscles before perturbation onset, 2) fewer early-phase activations at the internal oblique and gastrocnemius muscles, 3) fewer late-phase activations at the erector spinae, internal and external oblique, rectus abdominae, and tibialis anterior muscles, and 4) higher EMG amplitudes of the gastrocnemius muscle following the perturbation. The results indicate that a history of LBP associates with higher baseline muscle activation and that EMG responses are modulated from this activated state, rather than exhibiting acute burst activity from a quiescent state, perhaps to circumvent trunk displacements.     

Two stages and three components of the postural preparation to action

Previous studies of postural preparation to action/perturbation have primarily focused on anticipatory postural adjustments (APAs), the changes in muscle activation levels resulting in the production of net forces and moments of force. We hypothesized that postural preparation to action consists of two stages: (1) Early postural adjustments (EPAs), seen a few hundred ms prior to an expected external perturbation and (2) APAs seen about 100 ms prior to the perturbation. We also hypothesized that each stage consists of three components, anticipatory synergy adjustments seen as changes in covariation of the magnitudes of commands to muscle groups (M-modes), changes in averaged across trials levels of muscle activation, and mechanical effects such as shifts of the center of pressure. Nine healthy participants were subjected to external perturbations created by a swinging pendulum while standing in a semi-squatting posture. Electrical activity of twelve trunk and leg muscles and displacements of the center of pressure were recorded and analyzed. Principal component analysis was used to identify four M-modes within the space of muscle activations using indices of integrated muscle activation. This analysis was performed twice, over two phases, 400–700 ms prior to the perturbation and over 200 ms just prior to the perturbation. Similar robust results were obtained using the data from both phases. An index of a multi-M-mode synergy stabilizing the center of pressure displacement was computed using the framework of the uncontrolled manifold hypothesis. The results showed high synergy indices during quiet stance. Each of the two stages started with a drop in the synergy index followed by a change in the averaged across trials activation levels in postural muscles. There was a very long electromechanical delay during the early postural adjustments and a much shorter delay during the APAs. Overall, the results support our main hypothesis on the two stages and three components of the postural preparation to action/perturbation. This is the first study to document anticipatory synergy adjustments in whole-body tasks. We interpret the results within the referent configuration hypothesis (an extension of the equilibrium-point hypothesis): The early postural adjustment is based primarily on changes in the coactivation command, while the APAs involve changes in the reciprocal command. The results fit an earlier hypothesis that whole-body movements are controlled by a neuromotor hierarchy where each level involves a few-to-many mappings organized to stabilize its overall output.     

The influence of cues and stimulus history on the non-linear frequency characteristics of the pursuit response to randomized target motion

When humans pursue motion stimuli composed of alternating constant velocity segments of randomised duration (RD), they nevertheless initiate anticipatory eye deceleration before stimulus direction changes at a pre-programmed time based on averaging prior stimulus timing. We investigated, in both the time and frequency domains, how averaging interacts with deceleration cues by comparing responses to stimuli composed of segments that were either constant-velocity ramps or half-cycle sinusoids. RDs were randomized within 6 ranges, each comprising 8 RDs and having differing mean RD. In sine responses, deceleration cues could be used to modulate eye velocity for long-range stimuli (RD = 840–1,200 ms) but in the shortest range (RD = 240–660 ms) cues became ineffective, so that sine responses resembled ramp responses, and anticipatory timing was primarily dependent on averaging. Additionally, inclusion of short duration (240 ms) segments reduced peak eye velocity for all RDs within a range, even when longer RDs in the range (up to 1,080 ms) would normally elicit much higher velocities. These effects could be attributed to antagonistic interactions between visually driven pursuit components and pre-programmed anticipatory deceleration components. In the frequency domain, the changes in peak velocity and anticipatory timing with RD range were translated into non-linear gain and phase characteristics similar to those evoked by sum-of-sines stimuli. Notably, a reduction in pursuit gain occurred when high-frequency components associated with short duration segments were present. Results appear consistent with an adapted pursuit model, in which pre-programmed timing information derived from an internally reconstructed stimulus signal is stored in short-term memory and controls the initiation of predictive responses.     

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.     

Lateral balance organisation in human stance in response to a random or predictable perturbation

The effect of the predictability of perturbation to standing balance was evaluated in terms of the muscle activity and response dynamics of five subjects exposed to horizontal forces at the pelvis producing sideways or forward sway. Rapid (EMG onset latencies of 70–80 ms recorded from the left gluteus medius and gastrocnemius) and qualitatively different patterns of response were produced by forward pushes and pushes to either side. However, the EMG response to left push was constant in pattern and timing, whether the push direction was constant and, therefore, predictable over a block of trials or whether the left push trials were interleaved randomly with right push or forward push trials. Moreover, there were no systematic effects of perturbation direction uncertainty on the latency and rate of increase of ground reaction forces. We conclude that prior information does not speed postural responses that differ quantitatively according to the direction of perturbation to balance. Received: 13 October 1997 / Accepted: 17 July 1998     

Automatic postural responses in the cat: responses of hindlimb muscles to horizontal perturbations of stance in multiple directions

Summary The effect of the direction of unexpected horizontal perturbations of stance on the organization of automatic postural responses was studied in cats. We recorded EMG activity in eight proximal and distal muscles of the hindlimb along with vertical forces imposed by the limbs in awake behaving cats while they stood on an hydraulic platform. Postural responses to motion of the platform in 16 different horizontal directions were recorded. Vertical force changes were consistent with passive shifts of the center of mass and active correction of stance by the animals. When the perturbation was in the sagittal plane, vertical force changes began about 65 ms following initial platform movement. When the perturbation contained a component in the lateral direction, latency for vertical force changes was about 25 ms and an inflection in the vertical force trace was observed at 65 ms. No EMG responses were observed with latencies that were short enough to account for the early force component and it was concluded that this force change was due to passive shifts of the center of mass. The amplitude of the EMG responses of each muscle recorded varied systematically as perturbation direction changed. The directions for which an individual muscle showed measurable EMG activity were termed the muscle's angular range of activation. No angular range of activation was oriented strictly in the A-P or lateral directions. Most muscles displayed angular ranges of activation that encompassed a range of less than 180°. Onset latencies of EMG responses also varied systematically with perturbation direction. The amplitude and latency relationships between muscles, which made up the organization of postural responses, also varied systematically as perturbation direction was changed. This result suggests that direction of perturbation determines organizational makeup of postural responses, and for displacements in the horizontal plane, is considered a continuous variable by the nervous system.