The effects of trait and state anxiety on gait in healthy young adults.

Stable, personality-based (trait), and fluctuating, situational (state) anxiety have both been shown to consume attentional resources and reduce functional cognitive capacity, which may play a role in gait control. However, the role of attention in the relationship between trait and state anxiety has not yet been investigated formally. This study used a virtual reality-threat environment to evaluate whether changes in attention mediate the effects of state and trait anxiety on gait. Thirty adults aged 19-28 completed five walking trials in four conditions: (i) low threat-walking across a virtual plank (0.5 m wide) on flat ground; (ii) low threat + dual task (auditory digit monitoring); (iii) high threat-walking across a virtual plank elevated above a deep pit; and (iv) high threat + dual task. Trait anxiety levels were determined by the State-Trait Anxiety Inventory, while state anxiety was captured using self-assessment manikins. Higher trait anxiety predicted slower gait velocity and longer time in double support in the high-threat condition compared to low-threat condition (i vs iii), but not when dual tasking, compared to single-task walking, in the absence of threat (ii vs i). Additionally, higher trait anxiety predicted increased step length variability in the high compared to low-threat dual-task condition. Overall, trait anxiety predicts a slower, more cautious gait pattern during threatening conditions while dual tasking during the threat.

Increased Ability to Perceive Relevant Sensory Information Minimizes Low Back Exposures in Lifting.

We have previously shown evidence that some individuals seem to consistently minimize low back loads when lifting, while others do not. However, it is unknown why. Individual differences in ability to perceive relevant sensory information may explain differences in minimization of low back loads during lifting, consistent with considering load reduction in one's movement objective in an optimal feedback control theory framework. The purpose of this study was to investigate whether individuals' ability to perceive proprioceptive information (both force- and posture-senses) at the low back was associated with peak low back loads when performing generic or occupation-specific lifts. Seventy-two participants were recruited to perform 10 barbell (generic) and backboard (occupation-specific) lifts, while whole-body kinematics and ground reaction forces were collected. Peak low back compression and anteroposterior shear forces normalized to body mass were calculated as dependent variables. Both posture matching ability and force matching ability at the heavier force targets were associated with lower means and variability of peak low-back loads in both lift types, albeit with small effect sizes (R2 ≤ .17). These findings support the utility of an optimal feedback control theory framework to explore factors explaining interindividual differences in low back loads during lifting. Further, this evidence suggests improving proprioceptive ability may be a useful strategy in lift training programs designed for workplace injury prevention.

History-dependent muscle resistance to stretch remains high after small, posturally relevant pre-movements.

The contributions of intrinsic muscle fiber resistance during mechanical perturbations to standing and other postural behaviors are unclear. Muscle short-range stiffness is known to vary depending on the current level and history of the muscle's activation, as well as the muscle's recent movement history; this property has been referred to as history dependence or muscle thixotropy. However, we currently lack sufficient data about the degree to which muscle stiffness is modulated across posturally relevant characteristics of muscle stretch and activation. We characterized the history dependence of muscle's resistance to stretch in single, permeabilized, activated, muscle fibers in posturally relevant stretch conditions and activation levels. We used a classic paired muscle stretch paradigm, varying the amplitude of a 'conditioning' triangular stretch-shorten cycle followed by a 'test' ramp-and-hold imposed after a variable inter-stretch interval. We tested low (<15%), intermediate (15-50%) and high (>50%) muscle fiber activation levels, evaluating short-range stiffness and total impulse in the test stretch. Muscle fiber resistance to stretch remained high at conditioning amplitudes of <1% optimal fiber length, L0, and inter-stretch intervals of >1 s, characteristic of healthy standing postural sway. An ∼70% attenuation of muscle resistance to stretch was reached at conditioning amplitudes of >3% L0 and inter-stretch intervals of <0.1 s, characteristic of larger, faster postural sway in balance-impaired individuals. The thixotropic changes cannot be predicted solely on muscle force at the time of stretch. Consistent with the disruption of muscle cross-bridges, muscle resistance to stretch during behavior can be substantially attenuated if the prior motion is large enough and/or frequent enough.

Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics.

Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents - including movement history dependence, and nonlinear scaling with muscle stretch velocity - emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to 'encode' aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.

Interaction between muscle tone, short-range stiffness and increased sensory feedback gains explains key kinematic features of the pendulum test in spastic cerebral palsy: A simulation study.

The pendulum test is a sensitive clinical assessment of spasticity where the lower leg is dropped from the horizontal position and features of limb motion are recorded. Three key kinematic features are associated with the degree of severity of spasticity in children with cerebral palsy: decreased initial limb excursion, reduced number of limb oscillations, and a non-vertical resting limb angle. While spasticity is attributed to increased velocity-dependent resistance to motion, prior models simulating increased sensorimotor feedback of muscle velocity fail to explain the key pendulum test kinematic outcomes in spastic individuals. Here we hypothesized that increased muscle tone, causing a transient increase in muscle force, i.e. short-range stiffness, could account for reduced first swing excursion and non-vertical resting limb angle. We further hypothesized that hyperreflexia modeled based on muscle fiber force, and not velocity, feedback would be necessary to reduce the number of oscillations because of its interaction with transiently increased muscle force due to short-range stiffness. We simulated the lower leg as a torque-driven single-link pendulum. Muscle tone was modeled as a constant baseline joint torque, short-range stiffness torque was dependent on the level of muscle tone, and delayed sensory feedback torque to simulate reflex activity was based on either muscle velocity or force. Muscle tone and transient short-range stiffness were necessary to simulate decreased initial swing excursion and non-vertical resting leg angle. Moreover, the reduction in the number of oscillations was best reproduced by simulating stretch reflex activity in terms of force, and not velocity, feedback. Varying only baseline muscle torque and reflex gain, we simulated a range of pendulum test kinematics observed across different levels of spasticity. Our model lends insight into physiological mechanisms of spasticity whose contributions can vary on an individual-specific basis, and potentially across different neurological disorders that manifest spasticity as a symptom.

Increased human stretch reflex dynamic sensitivity with height-induced postural threat.

KEY POINTS: Threats to standing balance (postural threat) are known to facilitate soleus tendon-tap reflexes, yet the mechanisms driving reflex changes are unknown. Scaling of ramp-and-hold dorsiflexion stretch reflexes to stretch velocity and amplitude were examined as indirect measures of changes to muscle spindle dynamic and static function with height-induced postural threat. Overall, stretch reflexes were larger with threat. Furthermore, the slope (gain) of the stretch-velocity vs. short-latency reflex amplitude relationship was increased with threat. These findings are interpreted as indirect evidence for increased muscle spindle dynamic sensitivity, independent of changes in background muscle activity levels, with a threat to standing balance. We argue that context-dependent scaling of stretch reflexes forms part of a multisensory tuning process where acquisition and/or processing of balance-relevant sensory information is continuously primed to facilitate feedback control of standing balance in challenging balance scenarios. ABSTRACT: Postural threat increases soleus tendon-tap (t-) reflexes. However, it is not known whether t-reflex changes are a result of central modulation, altered muscle spindle dynamic sensitivity or combined spindle static and dynamic sensitization. Ramp-and-hold dorsiflexion stretches of varying velocities and amplitudes were used to examine velocity- and amplitude-dependent scaling of short- (SLR) and medium-latency (MLR) stretch reflexes as an indirect indicator of spindle sensitivity. t-reflexes were also performed to replicate previous work. In the present study, we examined the effects of postural threat on SLR, MLR and t-reflex amplitude, as well as SLR-stretch velocity scaling. Forty young-healthy adults stood with one foot on a servo-controlled tilting platform and the other on a stable surface. The platform was positioned on a hydraulic lift. Threat was manipulated by having participants stand in low (height 1.1 m; away from edge) then high (height 3.5 m; at the edge) threat conditions. Soleus stretch reflexes were recorded with surface electromyography and SLRs and MLRs were probed with fixed-amplitude variable-velocity stretches. t-reflexes were evoked with Achilles tendon taps using a linear motor. SLR, MLR and t-reflexes were 11%, 9.5% and 16.9% larger, respectively, in the high compared to low threat condition. In 22 out of 40 participants, SLR amplitude was correlated to stretch velocity at both threat levels. In these participants, the gain of the SLR-velocity relationship was increased by 36.1% with high postural threat. These findings provide new supportive evidence for increased muscle spindle dynamic sensitivity with postural threat and provide further support for the context-dependent modulation of human somatosensory pathways.

Influence of emotional stimuli on lower limb cutaneous reflexes during human gait.

Previous research has shown that cutaneous reflexes are modulated when walking with a threat to stability. It is unclear if this reflex modulation is purely related to the context of the imposed threat or if emotional changes associated with the threat exert an independent influence on reflex excitability. This study investigated the influence of emotional stimuli on lower limb cutaneous reflexes during treadmill walking. Twenty-eight healthy young adults walked at a self-selected pace while viewing pictures that manipulated emotional arousal and valence (confirmed with electrodermal and self-report measures). Throughout each trial, cutaneous reflexes were evoked by electrically stimulating the sural nerve at heel contact, mid-stance, or toe off. Surface electromyography of the ipsilateral soleus (SOL), medial gastrocnemius (MG), tibialis anterior (TA), biceps femoris (BF), and vastus lateralis (VL) was recorded to assess reflexes. Highly arousing pictures, independent of valence, significantly facilitated TA, and trended toward facilitating SOL and BF reflexes during mid-stance. Unpleasant pictures, independent of arousal, significantly reduced reflex amplitudes in BF during mid-stance and TA during toe off. While changes in background muscle activity and step cadence were observed, they did not correlate with reflex changes. This study provides the first evidence that emotional stimuli exert an independent influence on cutaneous reflex excitability during gait. As cutaneous reflexes contribute to stability during gait, these findings support the notion that emotional state influences important sensorimotor processes underlying balance control.

Both standing and postural threat decrease Achilles' tendon reflex inhibition from tendon electrical stimulation.

KEY POINTS: Golgi tendon organs (GTOs) and associated Ib reflexes contribute to standing balance, but the potential impacts of threats to standing balance on Ib reflexes are unknown. Tendon electrical stimulation to the Achilles' tendon was used to probe changes in Ib inhibition in medial gastrocnemius with postural orientation (lying prone vs. upright standing; experiment 1) and height-induced postural threat (standing at low and high surface heights; experiment 2). Ib inhibition was reduced while participants stood upright, compared to lying prone (42.2%); and further reduced when standing in the high, compared to low, threat condition (32.4%). These experiments will impact future research because they demonstrate that tendon electrical stimulation can be used to probe Ib reflexes in muscles engaged in standing balance. These results provide novel evidence that human short-latency GTO-Ib reflexes are dependent upon both task, as evidenced by changes with postural orientation, and context, such as height-induced postural threat during standing. ABSTRACT: Golgi tendon organ Ib reflexes are thought to contribute to standing balance control, but it is unknown if they are modulated when people are exposed to a postural threat. We used a novel application of tendon electrical stimulation (TStim) to elicit Ib inhibitory reflexes in the medial gastrocnemius, while actively engaged in upright standing balance, to examine (a) how Ib reflexes to TStim are influenced by upright stance, and (b) the effects of height-induced postural threat on Ib reflexes during standing. TStim evoked short-latency (<47 ms) inhibition apparent in trigger-averaged rectified EMG, which was quantified in terms of area, duration and mean amplitude of inhibition. In order to validate the use of TStim in a standing model, TStim-Ib inhibition was compared from conditions where participants were lying prone vs. standing upright. TStim evoked Ib inhibition in both conditions; however, significant reductions in Ib inhibition area (42.2%) and duration (32.9%) were observed during stance. Postural threat, manipulated by having participants stand at LOW (0.8 m high, 0.6 m from edge) and HIGH (3.2 m, at edge) elevated surfaces, significantly reduced Ib inhibition area (32.4%), duration (16.4%) and amplitude (24.8%) in the HIGH, compared to LOW, threat condition. These results demonstrate TStim is a viable technique for investigating Ib reflexes in standing, and confirm Ib reflexes are modulated with postural orientation. The novel observation of reduced Ib inhibition with elevated postural threat reveals that human Ib reflexes are context dependent, and the human Ib reflex pathways are modulated by threat or emotional processing centres of the CNS.

Postural threat influences vestibular-evoked muscular responses.

Standing balance is significantly influenced by postural threat. While this effect has been well established, the underlying mechanisms of the effect are less understood. The involvement of the vestibular system is under current debate, and recent studies that investigated the effects of height-induced postural threat on vestibular-evoked responses provide conflicting results based on kinetic (Horslen BC, Dakin CJ, Inglis JT, Blouin JS, Carpenter MG. J Physiol 592: 3671-3685, 2014) and kinematic (Osler CJ, Tersteeg MC, Reynolds RF, Loram ID. Eur J Neurosci 38: 3239-3247, 2013) data. We examined the effect of threat of perturbation, a different form of postural threat, on coupling (cross-correlation, coherence, and gain) of the vestibulo-muscular relationship in 25 participants who maintained standing balance. In the "No-Threat" conditions, participants stood quietly on a stable surface. In the "Threat" condition, participants' balance was threatened with unpredictable mediolateral support surface tilts. Quiet standing immediately before the surface tilts was compared to an equivalent time from the No-Threat conditions. Surface EMG was recorded from bilateral trunk, hip, and leg muscles. Hip and leg muscles exhibited significant increases in peak cross-correlation amplitudes, coherence, and gain (1.23-2.66×) in the Threat condition compared with No-Threat conditions, and significant correlations were observed between threat-related changes in physiological arousal and medium-latency peak cross-correlation amplitude in medial gastrocnemius (r = 0.408) muscles. These findings show a clear threat effect on vestibular-evoked responses in muscles in the lower body, with less robust effects of threat on trunk muscles. Combined with previous work, the present results can provide insight into observed changes during balance control in threatening situations. NEW & NOTEWORTHY: This is the first study to show increases in vestibular-evoked responses of the lower body muscles under conditions of increased threat of postural perturbation. While robust findings were observed in hip and leg muscles, less consistent results were found in muscles of the trunk. The present findings provide further support in the ongoing debate for arguments that vestibular-evoked balance responses are influenced by fear and anxiety and explain previous threat-related changes in balance.

Benefits of multi-session balance and gait training with multi-modal biofeedback in healthy older adults.

Real-time balance-relevant biofeedback from a wearable sensor can improve balance in many patient populations, however, it is unknown if balance training with biofeedback has lasting benefits for healthy older adults once training is completed and biofeedback removed. This study was designed to determine if multi-session balance training with and without biofeedback leads to changes in balance performance in healthy older adults; and if changes persist after training. 36 participants (age 60-88) were randomly divided into two groups. Both groups trained on seven stance and gait tasks for 2 consecutive weeks (3×/week) while trunk angular sway and task duration were monitored. One group received real-time multi-modal biofeedback of trunk sway and a control group trained without biofeedback. Training effects were assessed at the last training session, with biofeedback available to the feedback group. Post-training effects (without biofeedback) were assessed immediately after, 1-week, and 1-month post-training. Both groups demonstrated training effects; participants swayed less when standing on foam with eyes closed (EC), maintained tandem-stance EC longer, and completed 8 tandem-steps EC faster and with less sway at the last training session. Changes in sway and duration, indicative of faster walking, were also observed after training for other gait tasks. While changes in walking speed persisted post-training, few other post-training effects were observed. These data suggest there is little added benefit to balance training with biofeedback, beyond training without, in healthy older adults. However, transient use of wearable balance biofeedback systems as balance aides remains beneficial for challenging balance situations and some clinical populations.

Modulation of human vestibular reflexes with increased postural threat.

Anxiety and arousal have been shown to facilitate human vestibulo-ocular reflexes, presumably through direct neural connections between the vestibular nuclei and emotional processing areas of the brain. However, the effects of anxiety, fear and arousal on balance-relevant vestibular reflexes are currently unknown. The purpose of this study was to manipulate standing height to determine whether anxiety and fear can modulate the direct relationship between vestibular signals and balance reflexes during stance. Stochastic vestibular stimulation (SVS; 2-25 Hz) was used to evoke ground reaction forces (GRF) while subjects stood in both LOW and HIGH surface height conditions. Two separate experiments were conducted to investigate the SVS-GRF relationship, in terms of coupling (coherence and cumulant density) and gain, in the medio-lateral (ML) and antero-posterior (AP) directions. The short- and medium-latency cumulant density peaks were both significantly increased in the ML and AP directions when standing in HIGH, compared to LOW, conditions. Likewise, coherence was statistically greater between 4.3 Hz and 6.7 Hz in the ML, and between 5.5 and 17.7 Hz in the AP direction. When standing in the HIGH condition, the gain of the SVS-GRF relationship was increased 81% in the ML direction, and 231% in the AP direction. The significant increases in coupling and gain observed in both experiments demonstrate that vestibular-evoked balance responses are augmented in states of height-induced postural threat. These data support the possibility that fear or anxiety-mediated changes to balance control are affected by altered central processing of vestibular information.

Effects of postural threat on spinal stretch reflexes: evidence for increased muscle spindle sensitivity?

Standing balance is often threatened in everyday life. These threats typically involve scenarios in which either the likelihood or the consequence of falling is higher than normal. When cats are placed in these scenarios they respond by increasing the sensitivity of muscle spindles imbedded in the leg muscles, presumably to increase balance-relevant afferent information available to the nervous system. At present, it is unknown whether humans also respond to such postural threats by altering muscle spindle sensitivity. Here we present two studies that probed the effects of postural threat on spinal stretch reflexes. In study 1 we manipulated the threat associated with an increased consequence of a fall by having subjects stand at the edge of an elevated surface (3.2 m). In study 2 we manipulated the threat by increasing the likelihood of a fall by occasionally tilting the support surface on which subjects stood. In both scenarios we used Hoffmann (H) and tendon stretch (T) reflexes to probe the spinal stretch reflex circuit of the soleus muscle. We observed increased T-reflex amplitudes and unchanged H-reflex amplitudes in both threat scenarios. These results suggest that the synaptic state of the spinal stretch reflex is unaffected by postural threat and that therefore the muscle spindles activated in the T-reflexes must be more sensitive in the threatening conditions. We propose that this increase in sensitivity may function to satisfy the conflicting needs to restrict movement with threat, while maintaining a certain amount of sensory information related to postural control.

Influence of real and virtual heights on standing balance.

Fear and anxiety induced by threatening scenarios, such as standing on elevated surfaces, have been shown to influence postural control in young adults. There is also a need to understand how postural threat influences postural control in populations with balance deficits and risk of falls. However, safety and feasibility issues limit opportunities to place such populations in physically threatening scenarios. Virtual reality (VR) has successfully been used to simulate threatening environments, although it is unclear whether the same postural changes can be elicited by changes in virtual and real threat conditions. Therefore, the purpose of this study was to compare the effects of real and virtual heights on changes to standing postural control, electrodermal activity (EDA) and psycho-social state. Seventeen subjects stood at low and high heights in both real and virtual environments matched in scale and visual detail. A repeated measures ANOVA revealed increases with height, independent of visual environment, in EDA, anxiety, fear, and center of pressure (COP) frequency, and decreases with height in perceived stability, balance confidence and COP amplitude. Interaction effects were seen for fear and COP mean position; where real elicited larger changes with height than VR. This study demonstrates the utility of VR, as simulated heights resulted in changes to postural, autonomic and psycho-social measures similar to those seen at real heights. As a result, VR may be a useful tool for studying threat related changes in postural control in populations at risk of falls, and to screen and rehabilitate balance deficits associated with fear and anxiety.

Arousal, valence and their relative effects on postural control.

There is mounting evidence to suggest that emotional state can influence postural control. Emotions are often qualified using dimensions such as valence (pleasantness) and arousal. While affective pictures have been used to detail the effects of valence on postural control, the influence of arousal independently, or in combination with valence, has yet to be investigated. This is an important oversight because there are multiple sensory and neuromuscular mechanisms that are known to be sensitive to arousal and to contribute to postural control. As such, the current study is the first to independently manipulate valence and arousal through affective pictures and to examine their independent effects on postural control. Subjects stood quietly for 90 s long blocks while watching affective pictures, grouped by normative ratings of arousal (high and low) and valence (pleasant and unpleasant), and during which centre of pressure (COP) and electrodermal activity (EDA) were collected. EDA and anterior-posterior COP frequency were both increased with arousal, but not by valence. The postural effects observed in this study parallel those typically seen in other highly arousing situations, such as standing at the edge of an elevated platform or during performance evaluation. Therefore, we argue that arousal is a mediator of postural control and should be considered as a potential confound when testing or diagnosing subjects in clinical or experimental settings.

Human proprioceptive adaptations during states of height-induced fear and anxiety.

Clinical and experimental research has demonstrated that the emotional experience of fear and anxiety impairs postural stability in humans. The current study investigated whether changes in fear and anxiety can also modulate spinal stretch reflexes and the gain of afferent inputs to the primary somatosensory cortex. To do so, two separate experiments were performed on two separate groups of participants while they stood under conditions of low and high postural threat. In experiment 1, the proprioceptive system was probed using phasic mechanical stimulation of the Achilles tendon while simultaneously recording the ensuing tendon reflexes in the soleus muscle and cortical-evoked potentials over the somatosensory cortex during low and high threat conditions. In experiment 2, phasic electrical stimulation of the tibial nerve was used to examine the effect of postural threat on somatosensory evoked potentials. Results from experiment 1 demonstrated that soleus tendon reflex excitability was facilitated during states of height-induced fear and anxiety while the magnitude of the tendon-tap-evoked cortical potential was not significantly different between threat conditions. Results from experiment 2 demonstrated that the amplitudes of somatosensory-evoked potentials were also unchanged between threat conditions. The results support the hypothesis that muscle spindle sensitivity in the triceps surae muscles may be facilitated when humans stand under conditions of elevated postural threat, although the presumed increase in spindle sensitivity does not result in higher afferent feedback gain at the level of the somatosensory cortex.

Improving impaired balance function: real-time versus carry-over effects of prosthetic feedback.

This study investigated whether training with realtime prosthetic biofeedback (BF) of trunk sway induces a carry-over improvement in balance control once BF is removed. 12 healthy older adults and 7 uncompensated unilateral vestibular loss patients were tested. All participants performed a battery of 14 balance and gait tasks (pre-test) upon their initial lab visit during which trunk angular sway was measured at L1-3. They then received balance BF training on a subset of 7 tasks, three times per week, for two consecutive weeks. BF was provided using a multi-modal biofeedback system with graded vibrotactile, auditory, and visual cues in relation to subject-specific angular displacement thresholds. Performance on the battery of the 14 balance and gait tasks (without BF) was re-assessed immediately after the 2 week training period, as well as 1 week later to examine BF carry-over effects. Significant reductions in trunk angular displacement were observed with the real-time BF, compared to the pre-test trials. The effects of BF persisted when BF was removed immediately after the final training session. BF carry-over effects were less evident at one week post-training. This evidence supports the potential short-term effects of BF training in a limited number of tasks after the BF is removed in healthy elderly subjects and those with vestibular loss. However, the prospect for longer term (>1 week) effects of prosthetic training on balance control remains currently unknown.