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ELife Dec 2020Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle...
Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents - including movement history dependence, and nonlinear scaling with muscle stretch velocity - emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to 'encode' aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.
Topics: Animals; Computer Simulation; Female; Models, Biological; Movement; Muscle Contraction; Muscle Spindles; Rats; Rats, Wistar
PubMed: 33370235
DOI: 10.7554/eLife.55177 -
Journal of Anatomy Aug 2015The first descriptions of muscle spindles with intrafusal fibres containing striated myofibrils and nervous elements were given approximately 150 years ago. It took,... (Review)
Review
The first descriptions of muscle spindles with intrafusal fibres containing striated myofibrils and nervous elements were given approximately 150 years ago. It took, however, another 100 years to establish the presence of two types of intrafusal muscle fibres: nuclear bag and nuclear chain fibres. The present paper highlights primarily the contribution of Robert Banks in fibre typing of intrafusal fibres: the confirmation of the principle of two types of nuclear bag fibres in mammalian spindles and the variation in occurrence of a dense M-band along the fibres. Furthermore, this paper summarizes how studies from the Umeå University group (Laboratory of Muscle Biology in the Department of Integrative Medical Biology) on fibre typing and the structure and composition of M-bands have contributed to the current understanding of muscle spindle complexity in adult humans as well as to muscle spindle development and effects of ageing. The variable molecular composition of the intrafusal sarcomeres with respect to myosin heavy chains and M-band proteins gives new perspectives on the role of the intrafusal myofibrils as stretch-activated sensors influencing tension/stiffness and signalling to nuclei.
Topics: Aging; Animals; Connectin; Cytoskeleton; Elasticity; Humans; Muscle Development; Muscle Spindles; Myofibrils; Myosin Heavy Chains
PubMed: 26179023
DOI: 10.1111/joa.12338 -
Sheng Li Xue Bao : [Acta Physiologica... Dec 2022Muscle spindle is the key proprioceptor in skeletal muscles and plays important roles in many physiological activities, such as maintaining posture, regulating movement... (Review)
Review
Muscle spindle is the key proprioceptor in skeletal muscles and plays important roles in many physiological activities, such as maintaining posture, regulating movement and controlling speed variation. It has significant clinical relevance and is emerging as a promising therapeutic target for the treatment of motor functional impairment and metabolic diseases. In this review, we summarized muscle spindle distribution and the mechanism of mechanical signal transmission, and reviewed the research progress on morphological and structural characteristics of muscle spindles.
Topics: Muscle Spindles; Muscle, Skeletal; Clinical Relevance
PubMed: 36594392
DOI: No ID Found -
Pflugers Archiv : European Journal of... Jan 2015The focus of this review is on the principal sensory ending of the mammalian muscle spindle, known as the primary ending. The process of mechanosensory transduction in... (Review)
Review
The focus of this review is on the principal sensory ending of the mammalian muscle spindle, known as the primary ending. The process of mechanosensory transduction in the primary ending is examined under five headings: (i) action potential responses to defined mechanical stimuli-representing the ending's input-output properties; (ii) the receptor potential-including the currents giving rise to it; (iii) sensory-terminal deformation-measurable changes in the shape of the primary-ending terminals correlated with intrafusal sarcomere length, and what may cause them; (iv) putative stretch-sensitive channels-pharmacological and immunocytochemical clues to their identity; and (v) synaptic-like vesicles-the physiology and pharmacology of an intrinsic glutamatergic system in the primary and other mechanosensory endings, with some thoughts on the possible role of the system. Thus, the review highlights spindle stretch-evoked output is the product of multi-ionic receptor currents plus complex and sophisticated regulatory gain controls, both positive and negative in nature, as befits its status as the most complex sensory organ after the special senses.
Topics: Action Potentials; Afferent Pathways; Animals; Humans; Mechanotransduction, Cellular; Models, Biological; Muscle Contraction; Muscle Spindles; Reflex, Stretch; Stress, Mechanical
PubMed: 24888691
DOI: 10.1007/s00424-014-1536-9 -
Experimental Physiology Jan 2024Muscle spindles encode mechanosensory information by mechanisms that remain only partially understood. Their complexity is expressed in mounting evidence of various... (Review)
Review
Muscle spindles encode mechanosensory information by mechanisms that remain only partially understood. Their complexity is expressed in mounting evidence of various molecular mechanisms that play essential roles in muscle mechanics, mechanotransduction and intrinsic modulation of muscle spindle firing behaviour. Biophysical modelling provides a tractable approach to achieve more comprehensive mechanistic understanding of such complex systems that would be difficult/impossible by more traditional, reductionist means. Our objective here was to construct the first integrative biophysical model of muscle spindle firing. We leveraged current knowledge of muscle spindle neuroanatomy and in vivo electrophysiology to develop and validate a biophysical model that reproduces key in vivo muscle spindle encoding characteristics. Crucially, to our knowledge, this is the first computational model of mammalian muscle spindle that integrates the asymmetric distribution of known voltage-gated ion channels (VGCs) with neuronal architecture to generate realistic firing profiles, both of which seem likely to be of great biophysical importance. Results predict that particular features of neuronal architecture regulate specific characteristics of Ia encoding. Computational simulations also predict that the asymmetric distribution and ratios of VGCs is a complementary and, in some instances, orthogonal means to regulate Ia encoding. These results generate testable hypotheses and highlight the integral role of peripheral neuronal structure and ion channel composition and distribution in somatosensory signalling.
Topics: Animals; Muscle Spindles; Mechanotransduction, Cellular; Neurons; Ion Channels; Electrophysiological Phenomena; Mammals
PubMed: 36966478
DOI: 10.1113/EP091099 -
Cells, Tissues, Organs 2019We examined the six small lateral rotators of the hip joint, which is one of the most flexible joints and allows kinematically complex motions of the hindlimb, to...
We examined the six small lateral rotators of the hip joint, which is one of the most flexible joints and allows kinematically complex motions of the hindlimb, to elucidate the functional differentiation among these muscles and to test the hypothesis that species-specific characteristics in hindlimb use during locomotion are reflected in the muscle spindle density and in other parameters of the deep small hip joint rotators. For these purposes, we estimated the number of muscle spindles of the superior gemellus muscle (SG), inferior gemellus muscle, quadratus femoris muscle, obturator internus muscle (OI), obturator externus muscle, and piriformis muscle in three Japanese macaques and a gibbon, using 30-µm-thick serial sections throughout each muscle length after azan staining. The numbers of muscle spindles per 10,000 muscle fibers were determined to compare inter-muscle variation. The spindle density was highest in the SG and lowest in the OI in the Japanese macaques, suggesting that the SG, which is attached to the tendon of the OI, functions as a kinesiological monitor of the OI. On the other hand, SG the was missing in the gibbon, and the OI in the gibbon contained more spindles than that in the Japanese macaques. This suggests that the SG and the OI fused into one muscle in the gibbon. We postulate that the relative importance of the deep small hip rotator muscles differs between the Japanese macaques and gibbon and that the gibbon's muscles are less differentiated in terms of the spindle density, probably because this brachiating species uses its hindlimbs less frequently.
Topics: Animals; Haplorhini; Hindlimb; Hylobates; Macaca; Macaca fuscata; Muscle Fibers, Skeletal; Muscle Spindles; Primates; Thigh
PubMed: 31927538
DOI: 10.1159/000504958 -
Journal of Neurophysiology Aug 2018Muscle spindles are ubiquitous encapsulated mechanoreceptors found in most mammalian muscles. There are two types of endings, primary and secondary, and both are... (Review)
Review
Muscle spindles are ubiquitous encapsulated mechanoreceptors found in most mammalian muscles. There are two types of endings, primary and secondary, and both are sensitive to changes in muscle length and velocity, with the primary endings having a greater dynamic sensitivity. Unlike other mechanoreceptors in the somatosensory system, muscle spindles are unique in possessing motor innervation, via γ-motoneurons (fusimotor neurons), that control their sensitivity to stretch. Much of what we know about human muscles spindles comes from studying the behavior of their afferents via intraneural microelectrodes (microneurography) inserted into accessible peripheral nerves. We review the functional properties of human muscle spindles, comparing and contrasting with what we know about the functions of muscle spindles studied in experimental animals. As in the cat, many human muscle spindles possess a background discharge that is related to the degree of muscle stretch, but mean firing rates are much lower (~10 Hz). They can faithfully encode changes in muscle fascicle length in passive conditions, but higher level extraction of information is required by the central nervous system to measure changes in muscle length during muscle contraction. Moreover, although there is some evidence supporting independent control of human muscle spindles via fusimotor neurons, any effects are modest compared with the clearly independent control of fusimotor neurons observed in the cat.
Topics: Action Potentials; Animals; Humans; Motor Neurons, Gamma; Muscle Contraction; Muscle Spindles; Neurons, Afferent; Proprioception
PubMed: 29668385
DOI: 10.1152/jn.00071.2018 -
The Journal of Physiology May 2021
Topics: Humans; Motor Neurons, Gamma; Muscle Spindles; Proprioception
PubMed: 33749841
DOI: 10.1113/JP281595 -
Sheng Li Xue Bao : [Acta Physiologica... Feb 2013One of the most important and urgent issues in the field of space medicine is to reveal the potential mechanism underlying the disused muscle atrophy during the... (Review)
Review
One of the most important and urgent issues in the field of space medicine is to reveal the potential mechanism underlying the disused muscle atrophy during the weightlessness or microgravity environment. It will conduce to find out effective methods for the prevention and treatment of muscle atrophy during a long-term space flight. Increasing data show that muscle spindle discharges are significantly altered following the hindlimb unloading, suggesting a vital role in the progress of muscle atrophy. In the last decades, we have made a series of studies on changes in the morphological structure and function of muscle spindle following simulated weightlessness. This review will discuss our main results and related researches for understanding of muscle spindle activities during microgravity environment, which may provide a theoretic basis for effective prevention and treatment of muscle atrophy induced by weightlessness.
Topics: Animals; Hindlimb Suspension; Muscle Spindles; Muscle, Skeletal; Muscular Atrophy; Space Flight; Weightlessness Simulation
PubMed: 23426520
DOI: No ID Found -
The Journal of Physiology May 2021
Topics: Decerebrate State; Humans; Motor Neurons, Gamma; Muscle Spindles
PubMed: 33749822
DOI: 10.1113/JP281594