Shoulder reflexes.

Dynamic shoulder stability is dependent on muscular coordination and sensory inputs. In the shoulder, mechanoreceptors are found in the coracoacromial ligament, the rotator cuff tendons, the musculotendinous junctions of the rotator cuff and in the capsule. The number of receptors in the capsule is small compared to the number in the other shoulder structures. Proprioceptive information from numerous receptors in muscles and tendons is mediated via fast conducting nervefibers and probably contribute more to kinaestethic sensation than information from capsule and ligaments. Therefore it seems likely that the joint receptors have a more distinct role for the kinaestethic sense than muscle receptors. In cats a direct reflex from the afferents innervating the shoulder to the muscles around the shoulder has been presented. The reflex had an extremely short latency (2.7-3.1 ms). In man, a very long latency (300 ms) excitatory reflex has been found when nerves in the capsule were stimulated electrically during shoulder surgery. In addition, when the anterior-inferior capsule was excited in conscious humans with modest amplitude electrical stimuli during muscle activity, a strong inhibition was found with an average latency of 33 ms. Stimulation of the sensory nerves in the coracoacromial ligament has also been found to modify muscle activity strongly. Even though our understanding of the control of shoulder motion is incomplete, it is clear that sensory inputs can strongly modify muscle activity around the shoulder. This has implications for rehabilitation and shoulder surgery.     

Sensory – Motor control of ligaments and associated neuromuscular disorders

The ligaments were considered, over several centuries, as the major restraints of the joints, keeping the associated bones in position and preventing instability, e.g. their separation from each other and/or mal-alignment. This project, conducted over 25 years, presents the following hypothesis:

1. Ligaments are also major sensory organs, capable of monitoring relevant kinesthetic and proprioceptive data.

2. Excitatory and inhibitory reflex arcs from sensory organs within the ligaments recruit/de-recruit the musculature to participate in maintaining joint stability as needed by the movement type performed.

3. The synergy of the ligament and associated musculature allocates prominent role for muscles in maintaining joint stability.

4. The viscoelastic properties of ligaments and their classical responses to static and cyclic loads or movements such as creep, tension–relaxation, hysteresis and strain rate dependence decreases their effectiveness as joint restraint and stabilizers and as sensory organs and exposes the joint to injury.

5. Long-term exposure of ligaments to static or cyclic loads/movements in a certain dose-duration paradigms consisting of high loads, long loading duration, high number of load repetitions, high frequency or rate of loading and short rest periods develops acute inflammatory responses which require long rest periods to resolve. These inflammatory responses are associated with a temporary (acute) neuromuscular disorder and during such period high exposure to injury is present.

6. Continued exposure of an inflamed ligament to static or cyclic load may result in a chronic inflammation and the associated chronic neuromuscular disorder known as cumulative trauma disorder (CTD).

7. The knowledge gained from basic and applied research on the sensory – motor function of ligaments can be used as infrastructure for translational research; mostly for the development of “smart orthotic” systems for ligament deficient patients. Three such “smart orthosis”, for the knee and lumbar spine are described.

8. The knowledge gained from the basic and applied research manifests in new physiotherapy modalities for ligament deficient patients.

Ligaments, therefore, are important structures with significant impact on motor control and a strong influence on the quality of movement, safety/stability of the joint and potential disorders that impact the safety and health of workers and athletes.     

Are coupled rotations in the lumbar spine largely due to the osseo-ligamentous anatomy?--a modeling study

Prior studies have found that primary rotations in the lumbar spine are accompanied by coupled out-of-plane rotations. However, it is not clear whether these accompanying rotations are primarily due to passive (discs, ligaments and facet joints) or active (muscles) spinal anatomy. The aim of this study was to use a finite element (FE) model of the lumbar spine to predict three-dimensional coupled rotations between the lumbar vertebrae, due to passive spinal structures alone. The FE model was subjected to physiologically observed whole lumbar spine rotations about in vivo centres of rotation. Model predictions were validated by comparison of intra-discal pressures and primary rotations with in vivo measurements and these showed close agreement. Predicted coupled rotations matched in vivo measurements for all primary motions except lateral bending. We suggest that coupled rotations accompanying primary motions in the sagittal (flexion/extension) and transverse (axial rotation) planes are primarily due to passive spinal structures. For lateral bending the muscles most likely play a key role in the coupled rotation of the spine.     

Cruciate ligament reflexes.

The idea of muscular reflexes elicited from sensory nerves of the cruciate ligaments is more than 100 years old, but the existence of such reflexes has not been proven until the recent two decades. First in animal experiments, a muscular excitation could be elicited in the hamstrings when the anterior cruciate ligament (ACL) was pulled, and tension in the ligament caused activity of the gamma motor neurones of the muscles around the knee. Impulses from the sensory nerves in ACL were activated during motion of the knee, in particular overstretching and combined extension and rotation. In humans, proprioception in the knee is decreased after ACL rupture. By mechanical or electrical stimulation of the ACL, an excitation in the hamstrings muscles can be elicited. During muscular activity, stimulation of the ACL or PCL results in a clear inhibition of the ongoing activity, both during static isometric and isokinetic muscle work, and also during dynamic activity (gait). This inhibitory reflex subjectively resembled giving way. The latency of the reflex was short in animals (about 3 ms) and long in humans (60-120 ms), probably caused by differences in the experimental setup and between species. The long latency in humans makes it unlikely that it is a directly protective reflex. Instead it may be involved in the updating of motor programs. Further research may characterize the reflex in details and map its pathways. The existence of this reflex indicate that the cruciate ligaments have an afferent function, which influences knee dynamics.     

Role of knee ligaments in proprioception and regulation of muscle stiffness

Physiologic evidence for the sensory role of the knee joint ligaments are reviewed. The cruciate and collateral ligaments accomodate morphologically different sensory nerve endings with different capabilities of providing the central nervous system (CNS) with information not only about noxious and chemical stimuli but also about mechanical events, e.g., movement- and position-related stretches of the ligaments. Available data show that low-threshold joint/ligament receptor (i.e., mechanoreceptor) afferents evoke only weak and rare effects in skeletomotor neurons (α-motoneurons), whereas they frequently and powerfully influence fusimotor neurons (γ-motoneurons). The effects on the γ-muscle-spindle system in the muscles around the knee are so potent that even stretches of the cruciate ligaments at relatively moderate loads (not noxious) may induce major changes in responses of the muscle spindle afferents. As the activity in the primary muscle spindle afferents modifies stiffness in the muscles, the cruciate ligament receptors may, through the γ-muscle-spindle system, participate in regulation and preparatory adjustment of the stiffness of the muscles around the knee joint and thereby of knee joint stiffness. Thus, the sensory system of the cruciate ligaments is able to contribute significantly to the functional stability of the knee joint. The possible role of (ligamentous) joint receptors in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes is also discussed.     

Electromuscular incapacitation results from stimulation of spinal reflexes

Electronic stun devices (ESD) often used in law enforcement, military action or self defense can induce total body uncoordinated muscular activity, also known as electromuscular incapacitation (EMI). During EMI the subject is unable to perform purposeful or coordinated movements. The mechanism of EMI induction has not been reported, but has been generally thought to be direct muscle and nerve excitation from the fields generated by ESDs. To determine the neuromuscular mechanisms linking ESD to induction of EMI, we investigated EMI responses using an anesthetized pig model. We found that EMI responses to ESD application can best be simulated by simultaneous stimulation of motor and sensory peripheral nerves. We also found that application of local anesthetics limited the response of ESD to local muscle stimulation and abolished the total body EMI response. Stimulation of the pure sensory peripheral nerves or nerves that are primarily motor nerves induced muscle responses that are consistent with well defined spinal reflexes. These findings suggest that the mechanism of ESD‐induced EMI is mediated by excitation of multiple simultaneous spinal reflexes. Although direct motor‐neuron stimulation in the region of ESD contact may significantly add to motor reactions from ESD stimulation, multiple spinal reflexes appear to be a major, and probably the dominant mechanism in observed motor response. Bioelectromagnetics 30:411–421, 2009. © 2009 Wiley‐Liss, Inc.     

Studies on the distribution of calcitonin gene-related peptide-like and substance P-like immunoreactivities in rat hind limb muscles

Summary The tibialis anterior, extensor digitorum longus and soleus muscles in the rat were examined with respect to the presence of calcitonin gene-related peptide-like as well as substance P-like immunoreactivity. In some of the motor endplates in these muscles, identified by staining for acetylcholinesterase activity, calcitonin gene-related peptide-like immunoreactivity was detected, but in others it was not. Calcitonin gene-related peptide-like immunoreactivity was found to coexist with substance-P-like immunoreactivity in nerve fibres located outside and inside the capsule of the muscle spindles, as well as in nerve fibres located in nerve fascicles. These fibres presumably represent sensory nerve fibres. Calcitonin gene-related peptide-like immunoreactivity, but not substance P-like immunoreactivity, was also detected, in cap-like structures located on the surface of the intrafusal muscle fibres in the polar regions of the spindles, structures which are likely to correspond to motor plate endings. The observations suggest that calcitonin gene-related peptide is heterogeneously present in the endplates of rat hind limb muscles, and gives for the first time immunohistochemical evidence for the presence of calcitonin gene-related peptide and substance P in the innervation of muscle spindles.     

Load-sharing in the lumbosacral spine in neutral standing & flexed postures – A combined finite element and inverse static study

Understanding load-sharing in the spine during in-vivo conditions is critical for better spinal implant design and testing. Previous studies of load-sharing that considered actual spinal geometry applied compressive follower load, with or without moment, to simulate muscle forces. Other studies used musculoskeletal models, which include muscle forces, but model the discs by simple beams or spherical joints and ignore the articular facet joints.This study investigated load-sharing in neutral standing and flexed postures using a detailed Finite Element (FE) model of the ligamentous lumbosacral spine, where muscle forces, gravity loads and intra-abdominal pressure, as predicted by a musculoskeletal model of the upper body, are input into the FE model. Flexion was simulated by applying vertebral rotations following spine rhythm measured in a previous in-vivo study, to the musculoskeletal model. The FE model predicted intradiscal pressure (IDP), strains in the annular fibers, contact forces in the facet joints, and forces in the ligaments. The disc forces and moments were determined using equilibrium equations, which considered the applied loads, including muscle forces and IDP, as well as forces in the ligaments and facet joints predicted by the FE model. Load-sharing was calculated as the portion of the total spinal load carried along the spine by each individual spinal structure. The results revealed that spinal loads which increased substantially from the upright to the flexed posture were mainly supported by the discs in the upright posture, whereas the ligaments’ contribution in resisting shear, compression, and moment was more significant in the flexed posture.     

Biomechanical implications of lumbar spinal ligament transection

Many lumbar spine surgeries either intentionally or inadvertently damage or transect spinal ligaments. The purpose of this work was to quantify the previously unknown biomechanical consequences of isolated spinal ligament transection on the remaining spinal ligaments (stress transfer), vertebrae (bone remodelling stimulus) and intervertebral discs (disc pressure) of the lumbar spine. A finite element model of the full lumbar spine was developed and validated against experimental data and tested in the primary modes of spinal motion in the intact condition. Once a ligament was removed, stress increased in the remaining spinal ligaments and changes occurred in vertebral strain energy, but disc pressure remained similar. All major biomechanical changes occurred at the same spinal level as the transected ligament, with minor changes at adjacent levels. This work demonstrates that iatrogenic damage to spinal ligaments disturbs the load sharing within the spinal ligament network and may induce significant clinically relevant changes in the spinal motion segment.     

Evaluating the viscoelastic properties of biological tissues in a new way

In this paper, a new method for evaluating the viscoelastic properties of biological tissues such as tendons and ligaments is presented. This method obtains the complex modulus of these tissues to characterize their viscoelastic properties. With this method, the stresses and strains measured in time are first transformed (using FFT), and the complex modulus is then obtained. The complex modulus contains sufficient information about the viscoelastic characteristics of the biological tissues. With this method, the mechanical properties of biological tissues can be measured without making apriori assumptions regarding their structures, and the measurements can be made in real time.     

Neuromuscular manifestations of viscoelastic tissue degradation following high and low risk repetitive lumbar flexion

Cumulative lumbar disorder is common in individuals engaged in long term performance of repetitive and static occupational/sports activities with the spine. The triggering source and of the disorder, the tissues involved in the failure and the biomechanical, neuromuscular, and biological processes active in the initiation and development of the disorder are not known. The hypothesis is forwarded that static and repetitive (cyclic) lumbar flexion-extension and the associated repeated stretch of the various viscoelastic tissues (ligaments, fascia, facet capsule, discs, etc.) causes micro-damage in their collagen fibers followed by an acute inflammation, triggering pain and reflexive muscle spasms/hyper-excitability. Continued exposure to activities, over time, converts the acute inflammation into a chronic one, viscoelastic tissues remodeling/degeneration, modified motor control strategy and permanent disability. Changes in lumbar stability are expected during the development of the disorder. A series of experimental data from in-vivo feline is reviewed and integrated with supporting evidence from the literature to gain a valuable insight into the multi-factorial development of the disorder. Prolonged cyclic lumbar flexion-extension at high loads, high velocities, many repetitions and short in between rest periods induced transient creep/laxity in the spine, muscle spasms and reduced stability followed, several hours later, by an acute inflammation/tissue degradation, muscular hyper-excitability and increased stability. The major findings assert that viscoelastic tissues sub-failure damage is the source and inflammation is the process which governs the mechanical and neuromuscular characteristic symptoms of the disorder. A comprehensive model of the disorder is presented. The experimental data validates the hypothesis as well as provide insights into the development of potential treatment and prevention of the disorder.     

Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans.

Spinal reflexes have traditionally been treated as separate from voluntary movements. However, animal experiments since the 1950s and human experiments since the 1970s have documented that sensory activities in afferents from muscles, skin, and joints are integrated with descending motor commands at the level of common spinal interneurons. Two different roles of this sensorimotor integration at the spinal level may be discerned. First, sensory feedback evoked by the active muscles may help to drive the motoneurons. Second, external stimuli, such as sudden perturbations of a limb, may give rise to "error signals," which are integrated into the ongoing motor activity and form the basis of corrective responses. When interpreting experimental data, it is important to consider these two different roles. Application of external stimuli may provide little information about how the spinal cord integrates sensory feedback evoked as part of ongoing movements. The complexity of the spinal machinery that is activated by external stimuli also makes the interpretation of data obtained from experiments dealing with artificial external stimuli, such as electrical stimuli, difficult. Nevertheless, such experiments have provided and will continue to provide very valuable information about how the brain and spinal cord ensure coordination of muscle activity during voluntary movement. So far, spinal control mechanisms have only been investigated to a limited extent in relation to sports and occupational activities. Provided that researchers consider the methodological problems of the techniques and that they seek independent validation of the findings, this may be a very fruitful research field in the future.     

Somatosensory Event-related Potentials from Orofacial Skin Stretch Stimulation

Cortical processing associated with orofacial somatosensory function in speech has received limited experimental attention due to the difficulty of providing precise and controlled stimulation. This article introduces a technique for recording somatosensory event-related potentials (ERP) that uses a novel mechanical stimulation method involving skin deformation using a robotic device. Controlled deformation of the facial skin is used to modulate kinesthetic inputs through excitation of cutaneous mechanoreceptors. By combining somatosensory stimulation with electroencephalographic recording, somatosensory evoked responses can be successfully measured at the level of the cortex. Somatosensory stimulation can be combined with the stimulation of other sensory modalities to assess multisensory interactions. For speech, orofacial stimulation is combined with speech sound stimulation to assess the contribution of multi-sensory processing including the effects of timing differences. The ability to precisely control orofacial somatosensory stimulation during speech perception and speech production with ERP recording is an important tool that provides new insight into the neural organization and neural representations for speech.     

Development of the gin trap reflex inManduca sexta: a comparison of larval and pupal motor responses

1. Responses of motor neurons in larvae and pupae of Manduca sexta to stimulation of tactile sensory neurons were measured in both semi-intact, and isolated nerve cord preparations. These motor neurons innervate abdominal intersegmental muscles which are involved in the production of a general flexion reflex in the larva, and the closure reflex of the pupal gin traps. 2. Larval motor neurons respond to stimulation of sensory neurons innervating abdominal mechanosensory hairs with prolonged, tonic excitation ipsilaterally, and either weak excitation or inhibition contralaterally (Figs. 4A, 6). 3. Pupae respond to tactile stimulation of mechanosensory hairs within the gin traps with a rapid closure reflex. Motor neurons which innervate muscles ipsilateral to the stimulus exhibit a large depolarization, high frequency firing, and abrupt termination (Figs. 2, 4B). Generally, contralateral motor neurons fire antiphasically to the ipsilateral motor neurons, producing a characteristic triphasic firing pattern (Figs. 7, 8) which is not seen in the larva. 4. Pupal motor neurons can also respond to sensory stimulation with other types of patterns, including rotational responses (Fig. 3A), gin trap opening reflexes (Fig. 3B), and 'flip-flop' responses (Fig. 9). 5. Pupal motor neurons, like larval motor neurons, do not show oscillatory responses to tonic current injection, nor do motor neurons of either stage appear to interact synaptically with one another. Most pupal motor neurons also exhibit i-V properties similar to those of larval motor neurons (Table 1; Fig. 10). Some pupal motor neurons, however, show a marked non-linear response to depolarizing current injection (Fig. 11).     

The effects of long-standing limb loss on anatomical reorganization of the somatosensory afferents in the brainstem and spinal cord

We examined the terminations of sensory afferents in the brainstem and spinal cord of squirrel monkeys and prosimian galagos 4-8 years after a therapeutic forelimb or hindlimb amputation within 2 months of birth. In each animal, the distributions of labeled sensory afferent terminations from remaining body parts proximal to the limb stump were much more extensive than in normal animals. These sprouted afferents extended into the portions of the dorsal horn of the spinal cord as well as the cuneate and external cuneate nuclei of the brainstem (forelimb amputees) or spinal Clarke's column (hindlimb amputee) related to the amputated limb. Such reorganization in sensory afferents along with reorganization of the motor efferents to muscles (Wu and Kaas, J Neurosci 19 : 7679-7697, 1999, Neuron 28 : 967-978, 2000) may provide a basis for mislocated phantom sensations of missing forelimb movements accompanying actual shoulder movements during cortical stimulation or movement imagery in patients with amputations.     

The effects of long-standing limb loss on anatomical reorganization of the somatosensory afferents in the brainstem and spinal cord

We examined the terminations of sensory afferents in the brainstem and spinal cord of squirrel monkeys and prosimian galagos 4-8 years after a therapeutic forelimb or hindlimb amputation within 2 months of birth. In each animal, the distributions of labeled sensory afferent terminations from remaining body parts proximal to the limb stump were much more extensive than in normal animals. These sprouted afferents extended into the portions of the dorsal horn of the spinal cord as well as the cuneate and external cuneate nuclei of the brainstem (forelimb amputees) or spinal Clarke's column (hindlimb amputee) related to the amputated limb. Such reorganization in sensory afferents along with reorganization of the motor efferents to muscles (Wu and Kaas, J Neurosci 19: 7679-7697, 1999, Neuron 28: 967-978, 2000) may provide a basis for mislocated phantom sensations of missing forelimb movements accompanying actual shoulder movements during cortical stimulation or movement imagery in patients with amputations.     

Brain Regions Associated to a Kinesthetic Illusion Evoked by Watching a Video of One's Own Moving Hand

It is well known that kinesthetic illusions can be induced by stimulation of several sensory systems (proprioception, touch, vision…). In this study we investigated the cerebral network underlying a kinesthetic illusion induced by visual stimulation by using functional magnetic resonance imaging (fMRI) in humans. Participants were instructed to keep their hand still while watching the video of their own moving hand (Self Hand) or that of someone else''s moving hand (Other Hand). In the Self Hand condition they experienced an illusory sensation that their hand was moving whereas the Other Hand condition did not induce any kinesthetic illusion. The contrast between the Self Hand and Other Hand conditions showed significant activation in the left dorsal and ventral premotor cortices, in the left Superior and Inferior Parietal lobules, at the right Occipito-Temporal junction as well as in bilateral Insula and Putamen. Most strikingly, there was no activation in the primary motor and somatosensory cortices, whilst previous studies have reported significant activation in these regions for vibration-induced kinesthetic illusions. To our knowledge, this is the first study that indicates that humans can experience kinesthetic perception without activation in the primary motor and somatosensory areas. We conclude that under some conditions watching a video of one''s own moving hand could lead to activation of a network that is usually involved in processing copies of efference, thus leading to the illusory perception that the real hand is indeed moving.     

Chaotic and ordered processes mediating the knee-jerk reflex

In nerve chains that mediate tendon reflexes one can distinguish structured activity that represents the development of reflex excitation in response to muscle stretch and stochastic activity which is the result of fluctuations emerging in nerve structures. In analyzing neuron processes, one should consider also the factor of information whose carriers in nerve chains are structured and stochastic activities. A putative generator of fluctuations of muscle responses (possibly the main one) are cortex levels. Stochastic processes in neuron chains cause instability of the motor system at rest and in movement. Stochastic activity maintains the tone of skeletal muscles and affects the sensitivity of sensory systems via the mechanism of stochastic resonance.     

Glycerinated catch apparatus of sea urchin spines: the effects of cations on its mechanical properties and ultrastructure

Sea urchin spinal ligaments (the catch apparatus) were extracted with glycerin, and electron microscopic observations comfirmed that no cell membranes remained intact after glycerination. We studied the effects of cations (Na(+), K(+), Ca(2+), Mg(2+)) on the mechanical properties of the glycerinated ligaments. Monovalent cations decreased whereas divalent cations increased the viscosity of the ligaments. The ion dependencies were similar to previous results with detergent-extracted holothurian dermis, which suggests that the echinoid ligament shares a similar mechanism for changes in mechanical properties with other catch connective tissues. This provides evidence against the hypothesis of that muscles in the catch apparatus are responsible for the changes in mechanical properties of the ligament. Fine projections cross-bridging collagen fibrils were observed in the glycerin-extracted ligaments as well as in the intact ligaments. They were found in all the ionic conditions studied.     

Convergence of nociceptive information from temporomandibular joint and tooth pulp afferents on C1 spinal neurons in the rat

The aim of the present study was to test the hypothesis that there is a convergence of afferent inputs from the temporomandibular joint (TMJ) on C1 spinal neurons responding to electrical stimulation of the tooth pulp (TP). In 14 pentobarbital anesthetized rats, the extracellular single unit activity of 31 C1 spinal neurons and the amplitude in a digastric muscle electromyogram (n = 31) increased proportionally during 1.0-3.5 times the threshold for the jaw-opening reflex (JOR). Of 31 C1 spinal neurons responsive to TP afferents, 28 (approximately 90%) were also excited by electrical stimulation of the ipsilateral TMJ capsule. All neurons tested were divided into three categories of nociceptive specific, wide dynamic range and non-responsive as to their responsiveness to mechanical stimuli (pin prick and touch) of the somatic receptive field (skin of the face, neck, jaw and upper forearm) and TMJ capsule. Nineteen (68%) of 28 C1 spinal neurons received nociceptive information from C fibers of the TMJ capsule. These results suggest that there is a convergence of noxious information from the TMJ and TP afferents on the same C1 spinal neurons, which importantly contribute to pain perception from the TMJ region.