The Somatosensory System: Physiology and Models

To analyze and compare the structural and molecular features of classic proprioceptors like muscle spindles and Golgi tendon organs (GTOs) and putative proprioceptors (palisade endings) in sheep extraocular muscle (EOMs). The EOMs of four sheep were analyzed. Frozen sections or wholemount preparations of the samples were immunohistochemically labeled and analyzed by confocal laser scanning microscopy. Triple labeling with different combinations of antibodies against neurofilament, synaptophysin, and choline acetyltransferase (ChAT), as well as alpha-bungarotoxin and phalloidin, was performed. Microscopic anatomy of the nerve end organs was analyzed by transmission electron microscopy. The microscopic anatomy demonstrated that muscle spindles and GTOs had a perineural capsule and palisade endings a connective tissue capsule. Sensory nerve terminals in muscle spindles and GTOs contained only a few vesicles, whereas palisade nerve terminals were full of clear vesicles. Likewise, motor terminals in the muscle spindles' polar regions were full of clear vesicles. Immunohistochemistry showed that sensory nerve fibers as well as their sensory nerve terminals in muscle spindles and GTOs were ChAT-negative. Palisade endings were supplied by ChAT-positive nerve fibers, and the palisade complexes including palisade nerve terminals were also ChAT-immunoreactive. Motor terminals in muscle spindles were ChAT and alpha-bungarotoxin positive. The present study demonstrated in sheep EOMs that palisade endings are innervated by cholinergic axons exhibiting characteristics typical of motoneurons, whereas muscle spindles (except the polar regions) and GTOs are supplied by noncholinergic axons. These results raise the question of whether palisade endings are candidates for proprioceptors in EOMs.

Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat

Sensory contributions to stabilization of trunk posture in the sagittal plane

Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents

Across the human body, skeletal muscles have a broad range of biomechanical roles that employ complex proprioceptive control strategies to successfully execute a desired movement. This information is derived from peripherally located sensory apparatus, the muscle spindle and Golgi tendon organs. The abundance of these sensory organs, particularly muscle spindles, is known to differ considerably across individual muscles. Here we present a comprehensive data set of 119 muscles across the human body including architectural properties (muscle fibre length, mass, pennation angle and physiological cross-sectional area) and statistically test their relationships with absolute spindle number and relative spindle abundance (the residual value of the linear regression of the log-transformed spindle number and muscle mass). These data highlight a significant positive relationship between muscle spindle number and fibre length, emphasising the importance of fibre length as an input into the central nervous system. However, there appears to be no relationship between muscles architecturally optimised to function as displacement specialists and their provision of muscle spindles. Additionally, while there appears to be regional differences in muscle spindle abundance, independent of muscle mass and fibre length, our data provide no support for the hypothesis that muscle spindle abundance is related to anatomical specialisation.

Sensory afferent fibers are an important component of motor nerves and compose the majority of axons in many nerves traditionally thought of as "pure" motor nerves. These sensory afferent fibers innervate special sensory end organs in muscle, including muscle spindles that respond to changes in muscle length and Golgi tendons that detect muscle tension. Both play a major role in proprioception, sensorimotor extremity control feedback, and force regulation. After peripheral nerve injury, there is histological and electrophysiological evidence that sensory afferents can reinnervate muscle, including muscle that was not the nerve's original target. Reinnervation can occur after different nerve injury and muscle models, including muscle graft, crush, and transection injuries, and occurs in a nonspecific manner, allowing for cross-innervation to occur. Evidence of cross-innervation includes the following: muscle spindle and Golgi tendon afferent-receptor mismatch, vagal sensory fiber reinnervation of muscle, and cutaneous afferent reinnervation of muscle spindle or Golgi tendons. There are several notable clinical applications of sensory reinnervation and cross-reinnervation of muscle, including restoration of optimal motor control after peripheral nerve repair, flap sensation, sensory protection of denervated muscle, neuroma treatment and prevention, and facilitation of prosthetic sensorimotor control. This review focuses on sensory nerve regeneration and reinnervation in muscle, and the clinical applications of this phenomena. Understanding the physiology and limitations of sensory nerve regeneration and reinnervation in muscle may ultimately facilitate improvement of its clinical applications.

Unitary nerve impulses originating from slowly adapting muscle receptors were recorded with percutaneously inserted tungsten electrodes from the median and the tibial nerves in awake human subjects. Discharges from 72 receptors located in the wrist flexor muscles and the ankle extensor muscles were analysed. The possibilities to derive criteria of muscle spindles and Golgi tendon organs were tested by means of a number of experimental procedures. A differentiation between these two types of receptors could, for technical reasons, not be achieved by electrically induced muscle twitches. For the majority of the endings muscle spindle characteristics could be demonstrated. In relaxed muscles, a number of the muscle spindle afferents exhibited a high dynamic sensitivity to passive joint movements whereas a smaller proportion of them had a low dynamic sensitivity. A steady state discharge as a function of the muscle length could be demonstrated for some of them. During weak voluntary contractions without external muscle shortening, the majority of the units responded with a sustained impulse discharge which started and stopped almost simultaneously with the onset and the cessation of the extrafusal contractions. It was concluded that the motor cortex exerts a very powerful control of the intrafusal muscle fibres of the majority of the muscle spindles. For a few units the relation between the muscle force and the impulse frequency was very striking but for the majority of them this relation was poor. It was concluded that the former units were Golgi tendon organs.

BackgroundComplex regional pain syndrome (CRPS) may occur after trauma, usually to one limb, and is characterized by pain and disturbed blood flow, temperature regulation and motor control. Approximately 25% of cases develop fixed dystonia. Involvement of dysfunctional GABAergic interneurons has been suggested, however the mechanisms that underpin fixed dystonia are still unknown. We hypothesized that dystonia could be the result of aberrant proprioceptive reflex strengths of position, velocity or force feedback.MethodsWe systematically characterized the pattern of dystonia in 85 CRPS-patients with dystonia according to the posture held at each joint of the affected limb. We compared the patterns with a neuromuscular computer model simulating aberrations of proprioceptive reflexes. The computer model consists of an antagonistic muscle pair with explicit contributions of the musculotendinous system and reflex pathways originating from muscle spindles and Golgi tendon organs, with time delays reflective of neural latencies. Three scenarios were simulated with the model: (i) increased reflex sensitivity (increased sensitivity of the agonistic and antagonistic reflex loops); (ii) imbalanced reflex sensitivity (increased sensitivity of the agonistic reflex loop); (iii) imbalanced reflex offset (an offset to the reflex output of the agonistic proprioceptors).ResultsFor the arm, fixed postures were present in 123 arms of 77 patients. The dominant pattern involved flexion of the fingers (116/123), the wrists (41/123) and elbows (38/123). For the leg, fixed postures were present in 114 legs of 77 patients. The dominant pattern was plantar flexion of the toes (55/114 legs), plantar flexion and inversion of the ankle (73/114) and flexion of the knee (55/114).Only the computer simulations of imbalanced reflex sensitivity to muscle force from Golgi tendon organs caused patterns that closely resembled the observed patient characteristics. In parallel experiments using robot manipulators we have shown that patients with dystonia were less able to adapt their force feedback strength.ConclusionsFindings derived from a neuromuscular model suggest that aberrant force feedback regulation from Golgi tendon organs involving an inhibitory interneuron may underpin the typical fixed flexion postures in CRPS patients with dystonia.

3 - Features of the system for movement production

Chapter 6 - Receptors in Muscle and Their Role in Motor Control

Partial or total unilateral vestibular loss is the third most common cause of peripheral vestibular dysfunction. Dysfunction of one or both of the vestibular mechanisms can manifest physically as abnormalities of posture, balance, and/or visual acuity. This case report describes physical therapy examination and individualized intervention with vestibular rehabilitation for a patient with unilateral vestibular hypofunction. The patient was an 80-year-old male with electronystamographically confirmed unilateral vestibular loss of 98.3%. He demonstrated altered balance and gaze stability classifying him as having an increased risk for falling. After 5 weeks of individualized vestibular rehabilitation, the patient significantly decreased his fall risk from 11 to 20 of 24 on the Dynamic Gait Index. His gaze stability also improved from a 4 to 1 line disparity with dynamic visual acuity testing. The patient also had a decrease in perceived disability on the Dizziness Handicap Inventory from 30/100 at evaluation to 12/100 at discharge. Individualized vestibular rehabilitation decreased fall risk and improved gaze stability for a patient with significant unilateral vestibular hypofunction.

Neuroreceptors in the tissues of the knee joint

ObjectiveProprioception from extraocular muscles (EOMs) is important for proper visually‐guided behavior. Surprisingly, the classical proprioceptor pair (muscle spindles and Golgi tendon organs) is absent in the EOMs of most mammals and instead, palisade endings have been found in virtually all species analyzed so far. Due to their widespread distribution it is believed that palisade endings are candidates for EOM proprioception. We have analyzed the molecular profile and the central connection of palisade endings.MethodsWhole mount of cat EOMs were triple labeled with neuronal markers, including markers for cholinergic axons, exocytosis proteins, and acetylcholine receptors. In anterograde tracing experiments, neuronal tracer was injected into the EOM motor nuclei.ResultsPalisade endings were formed by nerve fibers that, coming from the muscle, extended into the tendon where they made a u‐shaped turn to approach the muscle tendon junction. Recurrent nerves divided into axonal branches and terminal varicosities to form palisade endings at the tip of single muscle fibers. Molecular analyses showed that palisade endings had a cholinergic phenotype because they expressed choline acetyl transferase, the synthesizing enzyme of acetylcholine. Additionally, palisade ending expressed SNAP25, synaptobrevin, synaptotagmin, complexin, and syntaxin, all of which are key proteins involved in neurotransmitter release. Acetylcholine esterase, the degrading enzyme of acetylcholine was absent in palisade ending and no receptors for cholinergic transmission were associated with palisade endings as demonstrated by the absence of alpha‐bungarotoxin signals. Following neuronal tracer injection in the EOM motor nuclei, palisade endings were labelled.ConclusionOur findings show that palisade endings are cholinergic, have an exocytosis machinery for neurotransmitter (acetylcholine) release and originate from the EOM motor nuclei. However, no receptors for cholinergic transmission are associated with palisade endings suggesting that palisade ending belong to an effector system that is different from that in other skeletal muscles.

Antagonist cocontraction of knee flexors during constant velocity muscle shortening and lengthening

The structures and distribution of encapsulated muscle receptors were examined in serial transverse sections of flexor carpi radialis in the adult cat. Four types of receptors (muscle spindles, Golgi tendon organs, paciniform, and Pacinian corpuscles) were identified. Their structures resembled those encountered in other limb muscles. Pacinian corpuscles were rare and occurred only in the external fascial coat of the muscle near its origin. The other three receptor types were distributed in an uneven but consistent pattern throughout the muscle. As noted previously (Gonyea and Ericson, '77), spindles were largely confined to a deep muscle region comprising less than 20% of the muscle volume, located directly between the long tendon of origin and the tendon of insertion. This region contains the largest proportion of type SO muscle fibers (Gonyea and Ericson, '77). Tendon organs and paciniform corpuscles were concentrated along the tendons that lined the spindle-rich muscle region. This region appeared to be composed of extrafusal fibers that were shorter and of more oblique pinnation than those in other regions. The localization of muscle receptors to the "oxidative" core of the muscle in its direct line of pull may have functional implications for afferent input to the spinal cord which are discussed. In addition, the possibility is raised that there are more paciniform corpuscles in flexor carpi radialis (and possibly other muscles) than previously thought.