Myomatrix arrays for high-definition muscle recording.

Neurons coordinate their activity to produce an astonishing variety of motor behaviors. Our present understanding of motor control has grown rapidly thanks to new methods for recording and analyzing populations of many individual neurons over time. In contrast, current methods for recording the nervous system's actual motor output - the activation of muscle fibers by motor neurons - typically cannot detect the individual electrical events produced by muscle fibers during natural behaviors and scale poorly across species and muscle groups. Here we present a novel class of electrode devices ('Myomatrix arrays') that record muscle activity at unprecedented resolution across muscles and behaviors. High-density, flexible electrode arrays allow for stable recordings from the muscle fibers activated by a single motor neuron, called a 'motor unit,' during natural behaviors in many species, including mice, rats, primates, songbirds, frogs, and insects. This technology therefore allows the nervous system's motor output to be monitored in unprecedented detail during complex behaviors across species and muscle morphologies. We anticipate that this technology will allow rapid advances in understanding the neural control of behavior and identifying pathologies of the motor system.

Cortical potentials time-locked to discrete postural events during quiet standing are facilitated during postural threat exposure.

During unperturbed bipedal standing, postural control is governed primarily by subcortical and spinal networks. However, it is unclear if cortical networks begin to play a greater role when stability is threatened. This study investigated how initial and repeated exposure to a height-related postural threat modulates cortical potentials time-locked to discrete centre of pressure (COP) events during standing. Twenty-seven young adults completed a series of 90-s standing trials at LOW (0.8 m above the ground, away from edge) and HIGH (3.2 m above the ground, at edge) threat conditions. Three LOW trials were completed before and after 15 consecutive HIGH trials. Participants stood on a force plate while electroencephalographic (EEG) activity was recorded. To examine changes in cortical activity in response to discrete postural events, prominent forward and backward peaks in the anterior-posterior COP time series were identified. EEG data were waveform-averaged to these events and the amplitude of event-related cortical activity was calculated. At the LOW condition, event-related potentials (ERPs) were scarcely detectable. However, once individuals stood at the HIGH condition, clear ERPs were observed, with more prominent potentials being observed for forward (edge-directed), compared to backward, COP events. Since forward COP peaks accelerate the centre of mass away from the platform edge, these results suggest there is intermittent recruitment of cortical networks that may be involved in the detection and minimization of postural sway toward a perceived threat. This altered cortical engagement appears resistant to habituation and may contribute to threat-related balance changes that persist following repeated threat exposure. KEY POINTS: While standing balance control is regulated primarily by subcortical and spinal processes, it is unclear if cortical networks play a greater role when stability is threatened. This study examined how cortical potentials time-locked to prominent peaks in the anterior-posterior centre of pressure (COP) time series were modulated by exposure to a height-related postural threat. While cortical potentials recorded over the primary sensorimotor cortices were scarcely detectable under non-threatening conditions, clear cortical potentials were observed when individuals stood under conditions of height-related threat. Cortical potentials were larger in response to COP peaks directed toward, compared to away from, the platform edge, and showed limited habituation with repeated threat exposure. Since forward COP peaks accelerate the centre of mass away from the platform edge, these findings suggest that when balance is threatened, there is intermittent recruitment of cortical networks, which may minimize the likelihood of falling in the direction of a perceived threat.

Myomatrix arrays for high-definition muscle recording.

Neurons coordinate their activity to produce an astonishing variety of motor behaviors. Our present understanding of motor control has grown rapidly thanks to new methods for recording and analyzing populations of many individual neurons over time. In contrast, current methods for recording the nervous system's actual motor output - the activation of muscle fibers by motor neurons - typically cannot detect the individual electrical events produced by muscle fibers during natural behaviors and scale poorly across species and muscle groups. Here we present a novel class of electrode devices ("Myomatrix arrays") that record muscle activity at unprecedented resolution across muscles and behaviors. High-density, flexible electrode arrays allow for stable recordings from the muscle fibers activated by a single motor neuron, called a "motor unit", during natural behaviors in many species, including mice, rats, primates, songbirds, frogs, and insects. This technology therefore allows the nervous system's motor output to be monitored in unprecedented detail during complex behaviors across species and muscle morphologies. We anticipate that this technology will allow rapid advances in understanding the neural control of behavior and in identifying pathologies of the motor system.

Toward Assessing the Functional Connectivity of Spinal Neurons.

Spinal interneurons play a critical role in motor output. A given interneuron may receive convergent input from several different sensory modalities and descending centers and relay this information to just as many targets. Therefore, there is a critical need to quantify populations of spinal interneurons simultaneously. Here, we quantify the functional connectivity of spinal neurons through the concurrent recording of populations of lumbar interneurons and hindlimb motor units in the in vivo cat model during activation of either the ipsilateral sural nerve or contralateral tibial nerve. Two microelectrode arrays were placed into lamina VII, one at L3 and a second at L6/7, while an electrode array was placed on the surface of the exposed muscle. Stimulation of tibial and sural nerves elicited similar changes in the discharge rate of both interneurons and motor units. However, these same neurons showed highly significant differences in prevalence and magnitude of correlated activity underlying these two forms of afferent drive. Activation of the ipsilateral sural nerve resulted in highly correlated activity, particularly at the caudal array. In contrast, the contralateral tibial nerve resulted in less, but more widespread correlated activity at both arrays. These data suggest that the ipsilateral sural nerve has dense projections onto caudal lumbar spinal neurons, while contralateral tibial nerve has a sparse pattern of projections.

Facilitation and Habituation of Cortical and Subcortical Control of Standing Balance Following Repeated Exposure to a Height-related Postural Threat.

Threats to stability elicit context-specific changes in balance control; however, the underlying neural mechanisms are not fully understood. Previous work has speculated that a shift toward greater supraspinal control may contribute to threat-related balance changes. This study investigated how neural correlates of cortical and subcortical control of balance were affected by initial and repeated exposure to a height-related postural threat. Corticomuscular coherence (CMC) between EEG recorded over the sensorimotor cortex and EMG recorded from the soleus (SOL) provided an estimate of cortical control, while intermuscular coherence (IMC) between bilateral SOL provided estimates of both cortical and subcortical control. These outcomes, along with measures of psychological and arousal state and standing balance control, were examined in 28 healthy young adults during a series of 90-s quiet standing trials completed at LOW (0.8 m above ground; away from edge) and HIGH (3.2 m above ground, at edge) threat conditions. Initial exposure to threat significantly increased gamma-band CMC (31-40 Hz) and IMC at frequencies thought to be mediated by cortical (21-40 Hz) and subcortical (5-20 Hz) substrates. Following repeated threat exposure, only estimates of cortical control (gamma CMC and 21-40 Hz IMC) demonstrated significant habituation. Estimates of cortical control changed in parallel with high-frequency centre of pressure power (>0.5 Hz) and plantar-dorsiflexor coactivation, but not other threat-related balance changes which did not habituate. These results support the hypothesis that postural threat induces a shift toward more supraspinal control of balance, and suggests this altered neural control may contribute to specific threat-related balance changes.

Initial experience of balance assessment introduces 'first trial' effects on emotional state and postural control.

BACKGROUND: Anxiety and arousal have been shown to influence balance control and, therefore, have the potential to confound balance assessment. It has been suggested that the 'first-trial' effect, where performance on the first trial of a balance task differs from subsequent trials, may be a result of participants being more anxious during their first experience of having their balance assessed. However, this remains speculative since limited work has simultaneously examined emotional state and balance control during repeated assessment of the same balance task. RESEARCH QUESTION: Determine how emotional state and standing balance control change over the course of repeated assessment. METHODS: Seventy-five healthy young adults completed five 120-s quiet standing trials. Psychological state was probed at each trial using self-report measures that assessed confidence, anxiety, and attention focus. Arousal was estimated from electrodermal activity and balance control was assessed from centre of pressure (COP) measures derived from forceplate data. Repeated measures ANOVAs were conducted to determine how each of these estimates changed with repeated testing. RESULTS: There were significant changes in emotional state with repeated testing; self-report and autonomic measures indicated that participants were most anxious and physiologically aroused during the first trial. This emotional response diminished with repeated testing, although the greatest changes occurred from the first to second trial. Despite these changes in emotional state, only some COP outcomes significantly changed. Individuals leaned further forward during only the first trial and demonstrated higher frequency and velocity mediolateral COP oscillations during the first two trials. SIGNIFICANCE: When balance is assessed for the first time in an unfamiliar laboratory setting, there is a transient emotional response which appears sufficient to influence some aspects of balance control. It is critical to control for these confounds when designing experiments or interventions involving balance assessment.

Selective preservation of changes to standing balance control despite psychological and autonomic habituation to a postural threat.

Humans exhibit changes in postural control when confronted with threats to stability. This study used a prolonged threat exposure protocol to manipulate emotional state within a threatening context to determine if any threat-induced standing behaviours are employed independent of emotional state. Retention of balance adaptations was also explored. Thirty-seven adults completed a series of 90-s standing trials at two surface heights (LOW: 0.8 m above ground, away from edge; HIGH: 3.2 m above ground, at edge) on two visits 2-4 weeks apart. Psychological and autonomic state was assessed using self-report and electrodermal measures. Balance control was assessed using centre of pressure (COP) and lower limb electromyographic recordings. Upon initial threat exposure, individuals leaned backward, reduced low-frequency centre of pressure (COP) power, and increased high-frequency COP power and plantar/dorsiflexor coactivation. Following repeated exposure, the psychological and autonomic response to threat was substantially reduced, yet only high-frequency COP power and plantar/dorsiflexor coactivation habituated. Upon re-exposure after 2-4 weeks, there was partial recovery of the emotional response to threat and few standing balance adaptations were retained. This study suggests that some threat-induced standing behaviours are coupled with the psychological and autonomic state changes induced by threat, while others may reflect context-appropriate adaptations resistant to habituation.

Adaptation of emotional state and standing balance parameters following repeated exposure to height-induced postural threat.

Height-induced postural threat influences standing balance control. However, it is unknown if minimizing individuals' emotional response to threat moderates this relationship. This study repeatedly exposed individuals to height-induced postural threat to determine if reducing the emotional response to threat influences standing balance control. Sixty-eight young adults completed a series of standing trials at LOW (0.8 m above ground, away from edge) and HIGH (3.2 m above ground, at edge) postural threat conditions. Emotional state was assessed using self-report and electrodermal measures. Standing balance was assessed through analysis of centre of pressure (COP) movement and lower leg electromyographic activity. Individuals' emotional response to threat was attenuated following repeated threat exposure. However, threat-induced changes in standing balance were largely preserved. When initially threatened, individuals leaned backward and demonstrated smaller amplitude and higher frequency of COP adjustments; these balance outcomes did not change following repeated threat exposure. Only high frequency COP oscillations (>1.8 Hz) and ankle muscle co-contraction showed any adaptation; regression analyses showed that these behavioural adaptations were accounted for by a combination of emotional and cognitive state changes. This suggests that some threat-induced standing balance changes are more closely linked with the emotional response to threat than others, and are therefore amendable to intervention.

Repeated exposure to the threat of perturbation induces emotional, cognitive, and postural adaptations in young and older adults.

Threat-related changes in postural control and their associations with changes in emotional and cognitive states are influenced by postural threat experience, however, limited work has explored individuals' capacity to adapt threat-related responses over longer periods of threat exposure. This study examined the effects of initial and repeated postural threat exposure on emotional, cognitive, and postural responses. Twenty-seven young and twenty-seven older adults stood on a force plate fixed to a translating platform. Threat was manipulated through expectation of a temporally and directionally (left or right) unpredictable platform perturbation. Participants completed one 60s stance trial with no expectation of perturbation (No Threat) followed by 24 trials with threat of perturbation (Threat). The stance period before each perturbation varied (5-60s) except on an early Threat trial and the last Threat trial (60s), which were used for analysis. Postural threat elicited similar emotional, cognitive, and postural changes in young and older adults. With initial threat exposure, participants reported increases in self-reported anxiety and physiological arousal, as well as broad changes in attention focus. Participants also significantly increased centre of pressure (COP) amplitude and frequency, and COP power within medium and high frequencies. With repeated threat exposure, anxiety, arousal, and some threat-induced changes in attention focus significantly adapted. These changes were accompanied by significant reductions in COP frequency and COP power within medium frequencies. Some emotional and cognitive outcomes returned to no threat levels while postural outcomes did not. This study suggests that some threat-related changes in standing postural control may be closely linked with one's emotional response to threat, while others may be context-dependent.

Exploring the relationship between threat-related changes in anxiety, attention focus, and postural control.

Individuals report directing attention toward and away from multiple sources when standing under height-related postural threat, and these changes in attention focus are associated with postural control modifications. As it is unknown whether these changes generalize to other types of threat situations, this study aimed to quantify changes in attention focus and examine their relationship with postural control changes in response to a direct threat to stability. Eighty young adults stood on a force plate fixed to a translating platform. Three postural threat conditions were created by altering the expectation of, and prior experience with, a postural perturbation: no threat of perturbation, threat without perturbation experience, and threat with perturbation experience. When threatened, participants were more anxious and reported directing more attention to movement processes, threat-related stimuli, and self-regulatory strategies, and less to task-irrelevant information. Postural sway amplitude and frequency increased with threat, with greater increases in frequency and smaller increases in amplitude observed with experience. Without experience, threat-related changes in postural control were accounted for by changes in anxiety; larger changes in anxiety were related to larger changes in sway amplitude. With experience, threat-related postural control changes were accounted for by changes in attention focus; increases in attention to movement processes were related to greater forward leaning and increases in sway amplitude, while increases in attention to self-regulatory strategies were related to greater increases in sway frequency. Results suggest that relationships between threat-related changes in anxiety, attention focus, and postural control depend on the context associated with the threat.

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.

Reliability of the diaphragmatic compound muscle action potential evoked by cervical magnetic stimulation and recorded via chest wall surface EMG.

INTRODUCTION: Stimulation of the phrenic nerve via cervical magnetic stimulation (CMS) elicits a compound muscle action potential (CMAP) that allows for assessment of diaphragm activation. The reliability of CMS to evoke the CMAP recorded by chest wall surface EMG has yet to be comprehensively examined. METHODS: CMS was performed on healthy young males (n=10) and females (n=10). Surface EMG electrodes were placed on the right and left hemi-diaphragm between the 6-8th intercostal spaces. CMAPs were analysed for: latency, duration, peak-to-peak amplitude, and area. Reliability within and between experimental sessions was assessed using intraclass correlation coefficients (ICC). Bilateral (right-left) and sex-based (male-female) comparisons were also made (independent samples t-test). RESULTS: All CMAP characteristics demonstrated high reproducibility within (ICCs>0.96) and between (ICCs>0.89) experimental sessions. No statistically significant bilateral or sex-based differences were found (p>0.05). DISCUSSION: CMS is a reliable and non-invasive method to evaluate phrenic nerve conduction.

Threat-induced changes in attention during tests of static and anticipatory postural control.

Postural threat, manipulated through changes in surface height, influences postural control. Evidence suggests changes in attention may contribute to this relationship. However, limited research has explored where and how attention is reallocated when threatened. The primary aim of this study was to describe changes in attention when presented with a postural threat, while a secondary aim was to explore associations between changes in attention and postural control. Eighty-two healthy young adults completed tests of static (quiet standing) and anticipatory (rise to toes) postural control under threatening and non-threatening conditions. Participants completed an open-ended questionnaire after each postural task which asked them to list what they thought about or directed their attention toward. Each item listed was assigned a percentage value reflecting how much attention it occupied. Exit interviews were completed to help confirm where attention was directed. Five attention categories were identified: movement processes, threat-relevant stimuli, self-regulatory strategies, task objectives, and task-irrelevant information. For both postural tasks, the percentage values and number of items listed for movement processes, threat-relevant stimuli, and self-regulatory strategies increased under threatening compared to non-threatening conditions, while the percentage values and number of items listed for task objectives and task-irrelevant information decreased. Changes in attention related to movement processes and self-regulatory strategies were associated with changes in static postural control, while changes in attention related to threat-relevant stimuli were associated with changes in anticipatory postural control. These results suggest that threat-induced changes in attention are multidimensional and contribute to changes in postural control.

Reliability of the Achilles tendon tap reflex evoked during stance using a pendulum hammer.

The tendon tap reflex (T-reflex) is often evoked in relaxed muscles to assess spinal reflex circuitry. Factors contributing to reflex excitability are modulated to accommodate specific postural demands. Thus, there is a need to be able to assess this reflex in a state where spinal reflex circuitry is engaged in maintaining posture. The aim of this study was to determine whether a pendulum hammer could provide controlled stimuli to the Achilles tendon and evoke reliable muscle responses during normal stance. A second aim was to establish appropriate stimulus parameters for experimental use. Fifteen healthy young adults stood on a forceplate while taps were applied to the Achilles tendon under conditions in which postural sway was constrained (by providing centre of pressure feedback) or unconstrained (no feedback) from an invariant release angle (50°). Twelve participants repeated this testing approximately six months later. Within one experimental session, tap force and T-reflex amplitude were found to be reliable regardless of whether postural sway was constrained (tap force ICC=0.982; T-reflex ICC=0.979) or unconstrained (tap force ICC=0.968; T-reflex ICC=0.964). T-reflex amplitude was also reliable between experimental sessions (constrained ICC=0.894; unconstrained ICC=0.890). When a T-reflex recruitment curve was constructed, optimal mid-range responses were observed using a 50° release angle. These results demonstrate that reliable Achilles T-reflexes can be evoked in standing participants without the need to constrain posture. The pendulum hammer provides a simple method to allow researchers and clinicians to gather information about reflex circuitry in a state where it is involved in postural control.

Personality traits and individual differences predict threat-induced changes in postural control.

This study explored whether specific personality traits and individual differences could predict changes in postural control when presented with a height-induced postural threat. Eighty-two healthy young adults completed questionnaires to assess trait anxiety, trait movement reinvestment (conscious motor processing, movement self-consciousness), physical risk-taking, and previous experience with height-related activities. Tests of static (quiet standing) and anticipatory (rise to toes) postural control were completed under low and high postural threat conditions. Personality traits and individual differences significantly predicted height-induced changes in static, but not anticipatory postural control. Individuals less prone to taking physical risks were more likely to lean further away from the platform edge and sway at higher frequencies and smaller amplitudes. Individuals more prone to conscious motor processing were more likely to lean further away from the platform edge and sway at larger amplitudes. Individuals more self-conscious about their movement appearance were more likely to sway at smaller amplitudes. Evidence is also provided that relationships between physical risk-taking and changes in static postural control are mediated through changes in fear of falling and physiological arousal. Results from this study may have indirect implications for balance assessment and treatment; however, further work exploring these factors in patient populations is necessary.

A method to investigate discrepancies between perceived and actual balance in older women.

Despite the established relationship between low balance confidence and poorer balance and gait performance, discrepancies may occur between an individual's perceived and actual abilities. This study determined if trunk sway measures could assist in identifying potential discrepancies between perceived and actual balance. Older women completed the Activities-specific Balance Confidence (ABC) scale and performed a series of 16 stance, gait and tandem gait tasks. Duration (or completed steps for tandem gait tasks) and trunk pitch and roll angle and angular velocity were calculated. Low (mean ABC score≤70%, n=33) and high (mean ABC score≥90%, n=99) balance confidence groups were identified from a pool of 204 participants. The low balance confidence group had greater stance trunk pitch and roll sway, shorter one leg stance durations, reduced gait trunk roll sway, longer gait durations, less tandem gait trunk roll sway and completed fewer tandem gait steps compared to the high balance confidence group. Stepwise linear discriminant analysis identified four variables that were used to achieve a classification accuracy of 75.8% for low and 90.9% for high balance confidence groups. This study reinforces the influence of low balance confidence on stance and gait control and provides direction for the identification and treatment of individuals with discrepancies between perceived and actual balance.