Billy L. Luu

The fusimotor and reafferent origin of the sense of force and weight

Non‐technical summary  Signals generated by the brain are thought to create the sensation of heaviness when we lift an object. We show here that signals arising from the body underlie this sensation. We fatigued the thumb muscles to half strength and had subjects lift a weight. Two subjects without sensation from the body said it felt twice as heavy, as expected by the central‐signal theory. However, normal subjects felt that the weight was lighter, inconsistent with the central‐signal theory. When we paralysed the muscles with curare and let them recover to half‐strength, the weights felt lighter despite the greater central signal. This is explained by smaller signals returning from muscle spindles because they have also been paralysed by the curare. Thus, peripheral signals with a major contribution from muscle spindles normally create the sense of heaviness. It also shows that muscle spindles provide more than information about limb position and movement.

Frequency-Specific Modulation of Vestibular-Evoked Sway Responses in Humans

Galvanic vestibular stimulation (GVS) results in characteristic muscle and whole-body responses in humans maintaining standing balance. However, the relationship between these two vestibular-evoked responses remains elusive. This study seeks to determine whether mechanical filtering from conversion of lower-limb muscle activity to body sway, during standing balance, can be used to attenuate sway while maintaining biphasic lower-limb muscle responses using frequency-limited stochastic vestibular stimulation (SVS). We hypothesized that SVS deprived of frequencies <2 Hz would evoke biphasic muscle responses with minimal whole-body sway due to mechanical filtering of the higher-frequency muscle responses. Subjects were exposed to five stimulus bandwidths: two meant to induce sway responses (0-1 and 0-2 Hz) and three to dissociate vestibular-evoked muscle responses from whole-body sway (0-25, 1-25, and 2-25 Hz). Two main results emerged: 1) SVS-related sway was attenuated when frequencies <2 Hz were excluded, whereas multiphasic muscle and force responses were retained; and 2) the gain of the estimated transfer functions exhibited successive low-pass filtering of vestibular stimuli during conversion to muscle activity, anteroposterior (AP) moment, and sway. This successive low-pass filtering limited the transfer of signal power to frequencies <20 Hz in muscle activity, <5 Hz in AP moment, and <2 Hz in AP trunk sway. Consequently, the present results show that SVS delivered at frequencies >2 Hz to standing humans do not cause a destabilizing whole-body sway response but are associated with the typical biphasic lower-limb muscle responses.

Absence of lateral gastrocnemius activity and differential motor unit behavior in soleus and medial gastrocnemius during standing balance.

In a standing position, the vertical projection of the center of mass passes in front of the ankle, which requires active plantar-flexor torque from the triceps surae to maintain balance. We recorded motor unit (MU) activity in the medial (MG) and lateral (LG) gastrocnemius muscle and the soleus (SOL) in standing balance and voluntary isometric contractions to understand the effect of functional requirements and descending drive from different neural sources on motoneuron behavior. Single MU activity was recorded in seven subjects with wire electrodes in the triceps surae. Two 3-min standing balance trials and several ramp-and-hold contractions were performed. Lateral gastrocnemius MU activity was rarely observed in standing. The lowest thresholds for LG MUs in ramp contractions were 20-35 times higher than SOL and MG MUs (P < 0.001). Compared with MUs from the SOL, MG MUs were intermittently active (P < 0.001), had higher recruitment thresholds (P = 0.022), and greater firing rate variability (P < 0.001); this difference in firing rate variability was present in standing balance and isometric contractions. In SOL and MG MUs, both recruitment of new MUs (R(2) = 0.59-0.79, P < 0.01) and MU firing rates (R(2) = 0.05-0.40, P < 0.05) were associated with anterior-posterior and medio-lateral torque in standing. Our results suggest that the two heads of the gastrocnemius may operate in different ankle ranges with the larger MG being of primary importance when standing, likely due to its fascicle orientation. These differences in MU discharge behavior were independent of the type of descending neural drive, which points to a muscle-specific optimization of triceps surae motoneurons.

Human standing is modified by an unconscious integration of congruent sensory and motor signals

•  Electrical vestibular stimulation delivered at the mastoid processes evokes a reflex response in the appendicular muscles only when they are actively involved in keeping the unsupported head and body balanced. •  We show that the vestibular‐evoked muscle response was present during a task that simulated the control of standing where sensory feedback was congruent with the motor‐generated expectation to balance the body, and absent when sensory feedback did not match. •  The present results indicate that the task dependency of the vestibular‐evoked muscle response relies on congruent sensory and motor signals, and that this is organised in the absence of a conscious perception of postural control. •  These findings help us understand how our brain combines sensory and motor signals to provide an internal representation of standing balance that can be used to assess whether a perturbation poses a postural threat.

Rectification is required to extract oscillatory envelope modulation from surface electromyographic signals

Rectification of surface electromyographic (EMG) recordings prior to their correlation with other signals is a widely used form of preprocessing. Recently this practice has come into question, elevating the subject of EMG rectification to a topic of much debate. Proponents for rectifying suggest it accentuates the EMG spike timing information, whereas opponents indicate it is unnecessary and its nonlinear distortion of data is potentially destructive. Here we examine the necessity of rectification on the extraction of muscle responses, but for the first time using a known oscillatory input to the muscle in the form of electrical vestibular stimulation. Participants were exposed to sinusoidal vestibular stimuli while surface and intramuscular EMG were recorded from the left medial gastrocnemius. We compared the unrectified and rectified surface EMG to single motor units to determine which method best identified stimulus-EMG coherence and phase at the single-motor unit level. Surface EMG modulation at the stimulus frequency was obvious in the unrectified surface EMG. However, this modulation was not identified by the fast Fourier transform, and therefore stimulus coherence with the unrectified EMG signal failed to capture this covariance. Both the rectified surface EMG and single motor units displayed significant coherence over the entire stimulus bandwidth (1-20 Hz). Furthermore, the stimulus-phase relationship for the rectified EMG and motor units shared a moderate correlation (r = 0.56). These data indicate that rectification of surface EMG is a necessary step to extract EMG envelope modulation due to motor unit entrainment to a known stimulus.

Validation of a Robotic Balance System for Investigations in the Control of Human Standing Balance

Previous studies have shown that human body sway during standing approximates the mechanics of an inverted pendulum pivoted at the ankle joints. In this study, a robotic balance system incorporating a Stewart platform base was developed to provide a new technique to investigate the neural mechanisms involved in standing balance. The robotic system, programmed with the mechanics of an inverted pendulum, controlled the motion of the body in response to a change in applied ankle torque. The ability of the robotic system to replicate the load properties of standing was validated by comparing the load stiffness generated when subjects balanced their own body to the robots mechanical load programmed with a low (concentrated-mass model) or high (distributed-mass model) inertia. The results show that static load stiffness was not significantly (p >; 0.05) different for standing and the robotic system. Dynamic load stiffness for the robotic system increased with the frequency of sway, as predicted by the mechanics of an inverted pendulum, with the higher inertia being accurately matched to the load properties of the human body. This robotic balance system accurately replicated the physical model of standing and represents a useful tool to simulate the dynamics of a standing person.

Transformation of Vestibular Signals for the Control of Standing in Humans.

During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscles ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances. SIGNIFICANCE STATEMENT The postural corrections critical to standing balance and navigation rely on transformation of sensory information into reference frames that are relevant for the required motor actions. Here, we demonstrate that the nervous system transforms vestibular sensory signals of head motion according to a muscles ability to stabilize the body along the direction of a vestibular-evoked disturbance. By manipulating the direction of the imposed vestibular signal relative to a muscles action, we show that the vestibular contribution to muscle activity is a highly flexible and organized balance response. This study provides insight into the neural integration and central processing associated with transformed vestibulomotor relationships that are essential to standing upright.

More conditioning stimuli enhance synaptic plasticity in the human spinal cord

OBJECTIVE To examine whether more paired corticospinal-motoneuronal stimulation (PCMS) is more effective at inducing spinal level plasticity. METHODS To produce facilitation, corticospinal volleys evoked by motor cortical transcranial magnetic stimulation (TMS) were timed to arrive at corticospinal-motoneuronal synapses prior to antidromic potentials evoked in motoneurones by electrical brachial plexus stimulation. Paired stimuli were delivered repeatedly. 50-pair conditioning (50-PCMS) was compared to 100 pairs in single block (100-PCMSsingle) and spaced (2 blocks of 50, 15-min break; 100-PCMSspaced) patterns, and to 50 single, unpaired TMS (50-TMS). Biceps responses to cervicomedullary stimulation (cervicomedullary motor evoked potentials, CMEPs) and TMS (motor evoked potentials, MEPs) were measured before and for 1h after conditioning (recorded each 5 min). RESULTS After 100-PCMS, average CMEP areas were increased by 46 ± 55% (mean ± SD; n=10; 100-PCMSsingle) and 71 ± 99% (100-PCMSspaced). 50-PCMS produced a non-significant 6 ± 40% increase. After 100-PCMSsingle and 100-PCMSspaced, CMEPs were larger than those after 50-TMS from 0 to 60 min (p<0.05). 100-PCMSsingle and 100-PCMSspaced produced more reliable changes than 50-PCMS. Overall, MEPs were larger at 35-60 min; however there were no differences between conditioning protocols. CONCLUSIONS More PCMS produces more reliable enhancement of corticospinal transmission. SIGNIFICANCE This technique has therapeutic potential to improve muscle control in patients with reduced descending drive.

Vestibular Contribution to Balance Control in the Medial Gastrocnemius and Soleus

The soleus (Sol) and medial gastrocnemius (mGas) muscles have different patterns of activity during standing balance and may have distinct functional roles. Using surface electromyography we previously observed larger responses to galvanic vestibular stimulation (GVS) in the mGas compared with the Sol muscle. However, it is unclear whether this difference is an artifact that reflects limitations associated with surface electromyography recordings or whether a compensatory balance response to a vestibular error signal activates the mGas to a greater extent than the Sol. In the present study, we compared the effect of GVS on the discharge behavior of 9 Sol and 21 mGas motor units from freely standing subjects. In both Sol and mGas motor units, vestibular stimulation induced biphasic responses in measures of discharge timing [11 ± 5.0 (mGas) and 5.6 ± 3.8 (Sol) counts relative to the sham (mean ± SD)], and frequency [0.86 ± 0.6 Hz (mGas), 0.34 ± 0.2 Hz (Sol) change relative to the sham]. Peak-to-trough response amplitudes were significantly larger in the mGas (62% in the probability-based measure and 160% in the frequency-based measure) compared with the Sol (multiple P < 0.05). Our results provide direct evidence that vestibular signals have a larger influence on the discharge activity of motor units in the mGas compared with the Sol. More tentatively, these results indicate the mGas plays a greater role in vestibular-driven balance corrections during standing balance.

Neurogenic changes in the upper airway of obstructive sleep apnoea.

Obstructive sleep apnoea (OSA) is linked to local neural injury that evokes airway muscle remodelling. The upper airway muscles of patients with OSA are exposed to intermittent hypoxia as well as vibration induced by snoring. A range of electrophysiological and other studies have established altered motor and sensory function of the airway in OSA. The extent to which these changes impair upper airway muscle function and their relationship to the progression of OSA remains undefined. This review will collate the evidence for upper airway remodelling in OSA, particularly the electromyographic changes in upper airway muscles of patients with OSA.