Short-latency Stretch Reflex Research Articles

Goal-directed modulation of stretch reflex gains is reduced in the non-dominant upper limb.

Most individuals experience their dominant arm as being more dexterous than the non-dominant arm, but the neural mechanisms underlying this asymmetry in motor behaviour are unclear. Using a delayed-reach task, we have recently demonstrated strong goal-directed tuning of stretch reflex gains in the dominant upper limb of human participants. Here, we used an equivalent experimental paradigm to address the neural mechanisms that underlie the preparation for reaching movements with the non-dominant upper limb. There were consistent effects of load, preparatory delay duration and target direction on the long latency stretch reflex. However, by comparing stretch reflex responses in the non-dominant arm with those previously documented in the dominant arm, we demonstrate that goal-directed tuning of short and long latency stretch reflexes is markedly weaker in the non-dominant limb. The results indicate that the motor performance asymmetries across the two upper limbs are partly due to the more sophisticated control of reflexive stiffness in the dominant limb, likely facilitated by the superior goal-directed control of muscle spindle receptors. Our findings therefore suggest that fusimotor control may play a role in determining performance of complex motor behaviours and support existing proposals that the dominant arm is better supplied than the non-dominant arm for executing more complex tasks, such as trajectory control.

Cancer survivors post-chemotherapy exhibit unimpaired short-latency stretch reflexes in the proximal upper extremity.

Oxaliplatin (OX) chemotherapy can lead to long-term sensorimotor impairments in cancer survivors. The impairments are often thought to be caused by OX-induced progressive degeneration of sensory afferents known as length-dependent dying-back sensory neuropathy. However, recent preclinical work has identified functional defects in the encoding of muscle proprioceptors and in motoneuron firing. These functional defects in the proprioceptive sensorimotor circuitry could readily impair muscle stretch reflexes, a fundamental building block of motor coordination. Given that muscle proprioceptors are distributed throughout skeletal muscle, defects in stretch reflexes could be widespread, including in the proximal region where dying-back sensory neuropathy is less prominent. All previous investigations on chemotherapy-related reflex changes focused on distal joints, leading to results that could be influenced by dying-back sensory neuropathy rather than more specific changes to sensorimotor circuitry. Our study extends this earlier work by quantifying stretch reflexes in the shoulder muscles in 16 cancer survivors and 16 healthy controls. Conduction studies of the sensory nerves in hand were completed to detect distal sensory neuropathy. We found no significant differences in the short-latency stretch reflexes (amplitude and latency) of the shoulder muscles between cancer survivors and healthy controls, contrasting with the expected differences based on the preclinical work. Our results may be linked to differences between the human and preclinical testing paradigms including, among many possibilities, differences in the tested limb or species. Determining the source of these differences will be important for developing a complete picture of how OX chemotherapy contributes to long-term sensorimotor impairments.NEW & NOTEWORTHY Our results showed that cancer survivors after oxaliplatin (OX) treatment exhibited stretch reflexes that were comparable with age-matched healthy individuals in the proximal upper limb. The lack of OX effect might be linked to differences between the clinical and preclinical testing paradigms. These findings refine our expectations derived from the preclinical study and guide future assessments of OX effects that may have been insensitive to our measurement techniques.

Assistive Loading Promotes Goal-Directed Tuning of Stretch Reflex Gains.

Voluntary movements are prepared before they are executed. Preparatory activity has been observed across the CNS and recently documented in first-order neurons of the human PNS (i.e., in muscle spindles). Changes seen in sensory organs suggest that independent modulation of stretch reflex gains may represent an important component of movement preparation. The aim of the current study was to further investigate the preparatory modulation of short-latency stretch reflex responses (SLRs) and long-latency stretch reflex responses (LLRs) of the dominant upper limb of human subjects. Specifically, we investigated how different target parameters (target distance and direction) affect the preparatory tuning of stretch reflex gains in the context of goal-directed reaching, and whether any such tuning depends on preparation duration and the direction of background loads. We found that target distance produced only small variations in reflex gains. In contrast, both SLR and LLR gains were strongly modulated as a function of target direction, in a manner that facilitated the upcoming voluntary movement. This goal-directed tuning of SLR and LLR gains was present or enhanced when the preparatory delay was sufficiently long (>250 ms) and the homonymous muscle was unloaded [i.e., when a background load was first applied in the direction of homonymous muscle action (assistive loading)]. The results extend further support for a relatively slow-evolving process in reach preparation that functions to modulate reflexive muscle stiffness, likely via the independent control of fusimotor neurons. Such control can augment voluntary goal-directed movement and is triggered or enhanced when the homonymous muscle is unloaded.

Short-latency stretch reflexes depend on the balance of activity in agonist and antagonist muscles during ballistic elbow movements.

The spinal stretch reflex is a fundamental building block of motor function, with a sensitivity that varies continuously during movement and when changing between movement and posture. Many have investigated task-dependent reflex sensitivity, but few have provided simple, quantitative analyses of the relationship between the volitional control and stretch reflex sensitivity throughout tasks that require coordinated activity of several muscles. Here, we develop such an analysis and use it to test the hypothesis that modulation of reflex sensitivity during movement can be explained by the balance of activity within agonist and antagonist muscles better than by activity only in the muscle homonymous with the reflex. Subjects completed hundreds of flexion and extension movements as small, pseudorandom perturbations of elbow angle were applied to obtain estimates of stretch reflex amplitude throughout the movement. A subset of subjects performed a postural control task with muscle activities matched to those during movement. We found that reflex modulation during movement can be described by background activity in antagonist muscles about the elbow much better than by activity only in the muscle homonymous to the reflex (P < 0.001). Agonist muscle activity enhanced reflex sensitivity, whereas antagonist activity suppressed it. Surprisingly, the magnitude of these effects was similar, suggesting a balance of control between agonists and antagonists very different from the dominance of sensitivity to homonymous activity during posture. This balance is due to a large decrease in sensitivity to homonymous muscle activity during movement rather than substantial changes in the influence of antagonistic muscle activity.NEW & NOTEWORTHY This study examined the sensitivity of the stretch reflexes elicited in elbow muscles to the background activity in these same muscles during movement and postural tasks. We found a heightened reciprocal control of reflex sensitivity during movement that was not present during maintenance of posture. These results help explain previous discrepancies in reflex sensitivity measured during movement and posture and provide a simple model for assessing their contributions to muscle activity in both tasks.

Significantly Delayed Medium-Latency Response of the Stretch Reflex in Delayed-Onset Muscle Soreness of the Quadriceps Femoris Muscles Is Indicative of Sensory Neuronal Microdamage.

Unaccustomed or strenuous eccentric exercise is known to cause delayed-onset muscle soreness. A recent hypothesis postulated that mechano-energetic microinjury of the primary afferent sensory neuron terminals in the muscle spindles, namely a transient Piezo2 channelopathy, could be the critical cause of delayed-onset muscle soreness in the form of a bi-phasic non-contact injury mechanism. This theory includes that this microlesion could delay the medium-latency response of the stretch reflex. Our aim with this study was to investigate this hypothesis. According to our knowledge, no study has examined the effect of delayed-onset muscle soreness on the medium-latency response of the stretch reflex. Our findings demonstrated that a significant delay in the medium-latency stretch reflex could be observed right after a multi-stage fitness test in the quadriceps femoris muscles of Hungarian professional handball players who consequently experienced delayed-onset muscle soreness. The long-latency stretch reflex and most likely short-latency stretch reflex were unaffected by delayed-onset muscle soreness in our study, which is in line with earlier findings. We translate these findings as indicative of proprioceptive Type Ia terminal microdamage in the muscle spindle in line with the aforementioned new acute non-contact compression axonopathy theory of delayed-onset muscles soreness.

Effect of short latency stretch reflex on passive and active muscle stiffness in the soleus muscle in vivo

The purpose of the present study was to determine the effect of the short latency stretch reflex on passive and active muscle stiffness in the soleus muscle. Fourteen males participated in this study. Passive muscle stiffness was calculated from passive muscle force and fascicle length during passive lengthening at four different angular velocities (5, 50, 100, and 200degs-1). Active muscle stiffness was also calculated according to changes in muscle force and fascicle length during fast lengthening at five different angular velocities (100, 200, 300, 500, and 600degs-1) after submaximal isometric contraction (30% of maximal voluntary contraction). During the measurements of passive and active muscle stiffness, the amplitude of the short latency stretch reflex in the soleus muscle was measured. Change in passive torque and passive muscle stiffness significantly increased, whereas change in the fascicle length decreased, as angular velocity increased. At 100 and 200degs-1 (stretch reflex responses were not observed at 5 and 50degs-1), the amplitude of the short latency stretch reflex was highly correlated with passive muscle stiffness. Change in torque and active muscle stiffness were highest at 100degs-1 and decreased as angular velocity increased. At all angular velocities under active conditions, the amplitude of the short latency stretch reflex was not correlated with active muscle stiffness. These results suggest that the short latency stretch reflex affects passive muscle stiffness in the soleus muscle, but not active muscle stiffness.

Test-Retest reliability of the internal shoulder rotator muscles' stretch reflex in healthy men

Until now the reproducibility of the short latency stretch reflex of the internal rotator muscles of the glenohumeral joint has not been identified. Twenty-three healthy male participants performed three sets of external shoulder rotation stretches with various pre-activation levels on two different dates of measurement to assess test–retest reliability. All stretches were applied with a dynamometer acceleration of 104°/s2 and a velocity of 150°/s. Electromyographical response was measured via surface EMG. Reflex latencies showed a pre-activation effect (ƞ2 = 0,355). ICC ranged from 0,735 to 0,909 indicating an overall “good” relative reliability. SRD 95% lay between ±7,0 to ±12,3 ms. The reflex gain showed overall poor test–retest reproducibility. The chosen methodological approach presented a suitable test protocol for shoulder muscles stretch reflex latency evaluation. A proof-of-concept study to validate the presented methodical approach in shoulder involvement including subjects with clinically relevant conditions is recommended.

Crosstalk opposing view: Independent fusimotor control of muscle spindles in humans: there is little to gain.

Crosstalk opposing view: Independent fusimotor control of muscle spindles in humans: there is little to gain.

Stepping onto the unknown: reflexes of the foot and ankle while stepping with perturbed perceptions of terrain.

Unanticipated variations in terrain can destabilize the body. The foot is the primary interface with the ground and we know that cutaneous reflexes provide important sensory feedback. However, little is known about the contribution of stretch reflexes from the muscles within the foot to upright stability. We used intramuscular electromyography measurements of the foot muscles flexor digitorum brevis (FDB) and abductor hallucis (AH) to show for the first time how their short-latency stretch reflex response (SLR) may play an important role in responding to stepping perturbations. The SLR of FDB and AH was highest for downwards steps and lowest for upwards steps, with the response amplitude for level and compliant steps in between. When the type of terrain was unknown or unexpected to the participant, the SLR of AH and the ankle muscle soleus tended to decrease. We found significant relationships between the contact kinematics and forces of the leg and the SLR, but a person's expectation still had significant effects even after accounting for these relationships. Motor control models of short-latency body stabilization should not only include local muscle dynamics, but also predictions of terrain based on higher level information such as from vision or memory.

Assessing Neural Connectivity and Associated Time Delays of Muscle Responses to Continuous Position Perturbations.

Both linear and nonlinear electromyographic (EMG) connectivity has been reported during the expression of stretch reflexes, though it is not clear whether they are generated by the same neural pathways. To answer this question, we aim to distinguish linear and nonlinear connectivity, as well as their delays in muscle responses, resulting from continuous elbow joint perturbations. We recorded EMG from Biceps Brachii muscle when eight able-bodied participants were performing a steady elbow flexion torque while simultaneously receiving a continuous position perturbation. Using a recently developed phase coupling metric, we estimated linear and nonlinear connectivity as well as their associated delays between Biceps EMG responses and perturbations. We found that the time delay for linear connectivity (24.5 ± 5.4ms) is in the range of short-latency stretch reflex period (< 35ms), while that for nonlinear connectivity (53.8 ± 3.2ms) is in the range of long-latency stretch reflex period (40-70ms). These results suggest that the estimated linear connectivity between EMG and perturbations is very likely generated by the mono-synaptic spinal stretch reflex loop, while the nonlinear connectivity may be associated with multi-synaptic supraspinal stretch reflex loops. As such, this study provides new evidence of the nature of neural connectivity related to the stretch reflex.

Spinal Circuits Mediate a Stretch Reflex Between the Upper Limbs in Humans

Inter-limb reflexes play an important role in coordinating behaviors involving different limbs. Previous studies have demonstrated that human elbow muscles express an inter-limb stretch reflex at long-latency (50–100 ms), a timing consistent with a trans-cortical linkage. Here we probe for inter-limb stretch reflexes in the shoulder muscles of human participants. Unexpected torque pulses displaced one or both shoulders while participants adopted a steady posture against background torques. The results demonstrated inter-limb stretch reflexes occurring at short-latency for both shoulder extensors and flexors; the rapid timing (36–50 ms) must involve a spinal linkage for the two arms. Inter-limb stretch reflexes were also observed at long-latency yet they were opposite to the preceding short-latency; when the short-latency stretch reflex was excitatory then the long-latency stretch reflex was inhibitory and vice versa. Comparing the responses to contralateral arm displacement to those during simultaneous displacement of both arms revealed that inhibitory inter-limb stretch reflexes are independent of within-limb stretch reflexes, but that excitatory inter-limb stretch reflexes are suppressed by within-limb stretch reflexes. Our results provide the first demonstration of short-latency inter-limb stretch reflexes in the upper limb of humans and reveal interacting spinal circuits for within-limb and inter-limb stretch reflexes.

A computer simulation study on the influences of loss and damage of primary muscle spindle afferents on soleus muscle stretch reflex.

Sensory loss is detrimental to sensorimotor control. Several studies have reported that loss and/or damage of primary (Ia) muscle spindle afferents significantly influence the stretch reflex responses of leg and foot muscles. However, a systematic experimental evaluation on how the impairment of Ia muscle spindle afferents affects the stretch reflex is difficult due to technical and ethical issues. In the present study, the aim was to use computer simulations of a multiscale neuromusculoskeletal model to investigate how changes in: i) the number of Ia afferents, ii) the synaptic conductance between Ia sensory fibers and spinal motor neurons (MNs), and iii) the conduction velocities (CVs) of Ia afferents, would influence the stretch reflex of a leg muscle (soleus). Simulation results showed that both anatomical and functional loss of Ia afferents exerted an influence on the amplitude of short-latency stretch reflex response (M1) and the late phase of medium-latency response (M2). Additionally, changes in CVs of Ia afferents mainly influenced the latency of M1 and the amplitude of M2. Our findings provide conceptual evidence that a combination of anatomical and functional loss, as well as changes in CVs of Ia afferents due to demyelination, can explain the stretch reflex responses observed in peripheral neuropathies.

Excessive short-latency stretch reflexes in the calf muscles do not cause postural instability in patients with hereditary spastic paraplegia

ObjectiveTo identify the role of hyperexcitable short-latency stretch reflexes (SLRs) on balance control in people with hereditary spastic paraplegia (PwHSP). MethodsSixteen PwHSP with triceps surae spasticity and 9 healthy control subjects were subjected to toes-up support-surface perturbations. EMG data were recorded from gastrocnemius, soleus and tibialis anterior. Furthermore, center-of-mass trajectories were recorded. ResultsPwHSP were less able to withstand the perturbations. Triceps surae SLRs (40–80 ms post perturbation) in PwHSP were increased compared to healthy subjects. Furthermore, a sustained triceps surae EMG activity at 220–320 ms post perturbation was observed in PwHSP, whereas control subjects demonstrated suppression of triceps surae activity. Center of mass trajectories started to diverge between PwHSP and controls only after ∼500 ms, with greater excursions being observed in the PwHSP. ConclusionsThe present results confirm that balance control is impaired in PwHSP. However, the late instant of center of mass divergence argues against a direct, causative role of hyperexcitable SLRs in the triceps surae. SignificanceWe postulate that enhanced short-latency stretch reflexes of the triceps surae do not underlie poor balance control in PwHSP. Instead, we suggest the lack of suppression of later triceps surae activity to be the main cause.

Statistical Considerations When Assessing Short Latency Stretch Reflexes in the Human Soleus Muscle.

The aim was to investigate trial-by-trial response characteristics in the short-latency stretch reflex (SSR). Fourteen dorsiflexion stretches were applied to the ankle joint with a pre-contracted soleus muscle on two days. The magnitude and variability of trial-by-trial responses of the SSR were assessed. The SSR was log-normally distributed and variance heterogeneous between subjects. For some subjects, the magnitude and variance differed between days and stretches. As velocity increased, variance heterogeneity tended to decrease and response magnitude increased. The current study demonstrates the need to assess trial-by-trial response characteristics and not averaged curves. Moreover, it provides an analysis of SSR characteristics accounting for log-normally distributed and variance heterogeneous trial-by-trial responses.

Triceps surae fascicle stretch is poorly correlated with short latency stretch reflex size

The short latency stretch reflex (SLR) is well described, but the stimulus that evokes the SLR remains elusive. One hypothesis states that reflex size is proportional to muscle fiber stretch, so in this study we examined the relationship between these 2 parameters in human triceps surae muscles. Achilles tendon taps and dorsiflexion stretches with different amplitudes and preactivation torques were applied to 6 participants while electromyography and muscle fascicle length changes were recorded in soleus and medial gastrocnemius (MG). In response to tendon taps, neither fascicle length nor velocity changes were correlated with SLR size in either muscle, but accelerometer peaks were observed immediately after hammer-tendon contact. Similar results were obtained after dorsiflexion stretches. Muscle fascicle stretch is poorly correlated with SLR size, regardless of perturbation parameters. We attribute the SLR trigger to the transmission of vibration through the lower limb, rather than muscle fiber stretch.

Differential modulation of motor cortex plasticity in skill- and endurance-trained athletes.

Extensive evidence exists that regular physical exercise offers neuroplastic benefits to the brain. In this study, exercise-specific effects on motor cortex plasticity were compared between 15 skilled and 15 endurance trained athletes and 8 controls. Plasticity was tested with a paired associative stimulation (PAS) protocol. PAS is a non-invasive stimulation method developed to induce bidirectional changes in the excitability of the cortical projections to the target muscles. Motor cortex excitability was assessed by motor-evoked potentials (MEPs) in the task-relevant soleus muscle, elicited with transcranial magnetic stimulation, before and following PAS. To test for changes at the spinal level, soleus short latency stretch reflexes (SLSR) were elicited before and after PAS. PAS induced a significant (76 ± 83 %) increase in MEP amplitude in the skill group, without significant changes in the endurance (-7 ± 35 %) or control groups (21 ± 30 %). Baseline MEP/post MEP ratio was significantly different between the skill and endurance groups. SLSR remained unchanged after the PAS intervention. The possible reason for differential motor cortex plasticity in skill and endurance groups is likely related to the different training-induced adaptations. The findings of the current study suggest that long-term skill training by skill group induced preferable adaptations in the task-related areas of the motor cortex because increased plasticity is known to enhance motor learning.

Statistical Considerations When Assessing Short Latency Stretch Reflexes in the Human Soleus Muscle.

The aim was to investigate trial-by-trial response characteristics in the short-latency stretch reflex (SSR). Fourteen dorsiflexion stretches were applied to the ankle joint with a precontracted soleus muscle on 2 days. The magnitude and variability of trial-by-trial responses of the SSR were assessed. The SSR was log-normally distributed and variance heterogeneous between subjects. For some subjects, the magnitude and variance differed between days and stretches. As velocity increased, variance heterogeneity tended to decrease and response magnitude increased. The current study demonstrates the need to assess trial-by-trial response characteristics and not averaged curves. Moreover, it provides an analysis of SSR characteristics accounting for log-normally distributed and variance heterogeneous trial-by-trial responses.

A Closed-Loop Brain–Computer Interface Triggering an Active Ankle–Foot Orthosis for Inducing Cortical Neural Plasticity

In this paper, we present a brain-computer interface (BCI) driven motorized ankle-foot orthosis (BCI-MAFO), intended for stroke rehabilitation, and we demonstrate its efficacy in inducing cortical neuroplasticity in healthy subjects with a short intervention procedure (∼15 min). This system detects imaginary dorsiflexion movements within a short latency from scalp EEG through the analysis of movement-related cortical potentials (MRCPs). A manifold-based method, called locality preserving projection, detected the motor imagery online with a true positive rate of 73.0 ± 10.3%. Each detection triggered the MAFO to elicit a passive dorsiflexion. In nine healthy subjects, the size of the motor-evoked potential (MEP) elicited by transcranial magnetic stimulation increased significantly immediately following and 30 min after the cessation of this BCI-MAFO intervention for ∼15 min ( p = 0.009 and , respectively), indicating neural plasticity. In four subjects, the size of the short latency stretch reflex component did not change following the intervention, suggesting that the site of the induced plasticity was cortical. All but one subject also performed two control conditions where they either imagined only or where the MAFO was randomly triggered. Both of these control conditions resulted in no significant changes in MEP size (p = 0.38 and p = 0.15). The proposed system provides a fast and effective approach for inducing cortical plasticity through BCI and has potential in motor function rehabilitation following stroke.

Decreased fibularis reflex response during inversion perturbations in FAI subjects

Investigate reflex responses in muscles throughout the lower limb and low back during sudden inversion perturbations in individuals with and without Functional Ankle Instability (FAI) while walking. Forty subjects participated in the study. Surface electromyogram recordings were obtained from the fibularis (FIB), gluteus medius (GM), erector spinae (ES), and sternocleidomastoid (SCM) of the injured/matched side as well as the uninjured/matched contralateral side (FIB_CLS, GM_CLS, or ES_CLS). Latency and amplitude data were collected while subjects were walking on a custom-built perturbation walkway. The onset of the short-latency stretch reflex of the FIB was significantly later in the injured side of the FAI individuals when compared to the control group (P=0.009). Both the short and long latency reflex amplitude was significantly smaller in the FIB muscle in the FAI group than in the control group (P<0.008). No significant differences in latency or amplitude reflex responses were identified between the two groups in the GM, ES, FIB_CLS, GM_CLS, or ES_CLS (P>.05). Interpretation of these results indicate that during a dynamic perturbation task individuals with FAI demonstrate longer fibularis muscle latencies on the injured side while no significant changes in the proximal muscle groups. Additionally, short and long latency reflex amplitude was significantly decreased in FAI individuals.

Anodal Transcranial Direct Current Stimulation (tDCS) Decreases the Amplitudes of Long-Latency Stretch Reflexes in Cerebellar Ataxia

Recent studies suggest that the neuromodulation of the cerebellum using transcranial direct current stimulation (tDCS) could represent a new therapeutic strategy for the management of cerebellar disorders. Anodal tDCS of the cerebellum increases the excitability of the cerebellar cortex. We tested the effects of anodal tDCS applied over the cerebellum in ataxic patients. We studied (a) stretch reflexes (SR) in upper limb (SLSR: short-latency stretch reflexes; LLSR: long-latency stretch reflexes), (b) a coordination functional task in upper limbs based on mechanical counters (MCT: mechanical counter test), and (c) computerized posturography. tDCS did not change the amplitude of SLSR, but reduced significantly the amplitudes of LLSR. tDCS did not improve the MCT scores and did not modify posture. We suggest that anodal tDCS of the cerebellum reduces the amplitudes of LLSR by increasing the inhibitory effect exerted by the cerebellar cortex upon cerebellar nuclei. The absence of effect upon upper limb coordination and posture suggests that the cerebello-cerebral networks subserving these functions are less responsive to anodal tDCS of the cerebellum. Anodal tDCS of the cerebellum represents a novel experimental tool to investigate the effects of the cerebellar cortex on the modulation of the amplitudes of LLSR.