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Experimental Physiology Jan 2024Hereditary sensory and autonomic neuropathy type III (HSAN III), also known as familial dysautonomia or Riley-Day syndrome, results from an autosomal recessive genetic... (Review)
Review
Hereditary sensory and autonomic neuropathy type III (HSAN III), also known as familial dysautonomia or Riley-Day syndrome, results from an autosomal recessive genetic mutation that causes a selective loss of specific sensory neurones, leading to greatly elevated pain and temperature thresholds, poor proprioception, marked ataxia and disturbances in blood pressure control. Stretch reflexes are absent throughout the body, which can be explained by the absence of functional muscle spindle afferents - assessed by intraneural microelectrodes inserted into peripheral nerves in the upper and lower limbs. This also explains the greatly compromised proprioception at the knee joint, as assessed by passive joint-angle matching. Moreover, there is a tight correlation between loss of proprioceptive acuity at the knee and the severity of gait impairment. Surprisingly, proprioception is normal at the elbow, suggesting that participants are relying more on sensory cues from the overlying skin; microelectrode recordings have shown that myelinated tactile afferents in the upper and lower limbs appear to be normal. Nevertheless, the lack of muscle spindles does affect sensorimotor control in the upper limb: in addition to poor performance in the finger-to-nose test, manual performance in the Purdue pegboard task is much worse than in age-matched healthy controls. Unlike those rare individuals with large-fibre sensory neuropathy, in which both muscle spindle and cutaneous afferents are absent, those with HSAN III present as a means of assessing sensorimotor control following the selective loss of muscle spindle afferents.
Topics: Humans; Muscle Spindles; Dysautonomia, Familial; Peripheral Nerves; Reflex, Stretch; Knee
PubMed: 37029664
DOI: 10.1113/EP090768 -
ELife Jul 2022Muscle spindles are encapsulated sensory organs found in most of our muscles. Prevalent models of sensorimotor control assume the role of spindles is to reliably encode...
Muscle spindles are encapsulated sensory organs found in most of our muscles. Prevalent models of sensorimotor control assume the role of spindles is to reliably encode limb posture and movement. Here, I argue that the traditional view of spindles is outdated. Spindle organs can be tuned by spinal γ motor neurons that receive top-down and peripheral input, including from cutaneous afferents. A new model is presented, viewing γ motor activity as an intermediate coordinate transformation that allows multimodal information to converge on spindles, creating flexible coordinate representations at the level of the peripheral nervous system. That is, I propose that spindles play a unique overarching role in the nervous system: that of a peripheral signal-processing device that flexibly facilitates sensorimotor performance, according to task characteristics. This role is compatible with previous findings and supported by recent studies with naturalistically active humans. Such studies have so far shown that spindle tuning enables the independent preparatory control of reflex muscle stiffness, the selective extraction of information during implicit motor adaptation, and for segmental stretch reflexes to operate in joint space. Incorporation of advanced signal-processing at the periphery may well prove a critical step in the evolution of sensorimotor control theories.
Topics: Adaptation, Physiological; Humans; Motor Neurons, Gamma; Movement; Muscle Spindles; Reflex
PubMed: 35829705
DOI: 10.7554/eLife.78091 -
Journal of Neurophysiology Mar 2018A method is described that, for the first time, allows instantaneous estimation of the Ia fiber input to human soleus motoneurons following electrical stimulation of the...
A method is described that, for the first time, allows instantaneous estimation of the Ia fiber input to human soleus motoneurons following electrical stimulation of the tibial nerve. The basis of the method is to determine the thresholds of the most and least excitable 1a fibers to electrical stimulation, and to treat the intervening thresholds as having a normal distribution about the mean; the validity of this approach is discussed. It was found that, for the same Ia fiber input, the percentage of soleus motoneurons contributing to the H (Hoffmann)-reflex differed considerably among subjects; when the results were pooled, however, there was an approximately linear relationship between Ia input and motoneuron output. Weak extension of the great toe diminished the soleus motoneuron reflex discharge in all but 2 of 16 subjects; the results for weak ankle plantarflexion were less consistent, but overall, there was a reduction in soleus motoneuron output also. The methodology should provide new insights into disorders of movement and tone, especially as it permits estimates of motoneuron depolarization to be made. NEW & NOTEWORTHY Assuming a normal distribution of Ia fiber thresholds to electrical stimulation and using the H-reflex, we determined for the first time an Ia input-α-motoneuron output relationship for the human soleus muscle. The relationship varies greatly among subjects but, overall, is approximately linear. Minimal contraction of a toe muscle alters the relationship dramatically, probably due to presynaptic inhibition of Ia fibers. Drawing on the literature, we can calculate changes in α-motoneuron membrane potential.
Topics: Action Potentials; Adult; Electric Stimulation; Female; H-Reflex; Humans; Male; Middle Aged; Motor Neurons; Muscle Spindles; Muscle, Skeletal; Nerve Fibers; Tibial Nerve; Young Adult
PubMed: 29187549
DOI: 10.1152/jn.00273.2017 -
The Journal of Experimental Biology Jan 2023Animals move across a wide range of surface conditions in real-world environments to acquire resources and avoid predation. To effectively navigate a variety of...
Animals move across a wide range of surface conditions in real-world environments to acquire resources and avoid predation. To effectively navigate a variety of surfaces, animals rely on several mechanisms including intrinsic mechanical responses, spinal-level central pattern generators, and neural commands that require sensory feedback. Muscle spindle Ia afferents play a critical role in providing sensory feedback and informing motor control strategies across legged vertebrate locomotion, which is apparent in cases where this sensory input is compromised. Here, we tested the hypothesis that spindle Ia afferents from hindlimb muscles are important for coordinating forelimb landing behavior in the cane toad. We performed bilateral sciatic nerve reinnervations to ablate the stretch reflex from distal hindlimb muscles while allowing for motor neuron recovery. We found that toads significantly delayed the onset and reduced the activation duration of their elbow extensor muscle following spindle Ia afferent ablation in the hindlimbs. However, reinnervated toads achieved similar elbow extension at touchdown to that of their pre-surgery state. Our results suggest that while toads likely tuned the activation timing of forelimb muscles in response to losing Ia afferent sensation from the hindlimbs they were likely able to employ compensatory strategies that allowed them to continue landing effectively with reduced sensory information during take-off. These findings indicate muscle spindle Ia afferents may contribute to tuning complex movements involving multiple limbs.
Topics: Animals; Muscle Spindles; Lower Extremity; Forelimb; Hindlimb; Bufo marinus
PubMed: 36576050
DOI: 10.1242/jeb.244629 -
Journal of Anatomy May 2022The platysma of the rhesus monkey consists of two parts: a platysma myoides located similar to the human platysma, and a platysma cervicale passing the dorsal cervical...
The platysma of the rhesus monkey consists of two parts: a platysma myoides located similar to the human platysma, and a platysma cervicale passing the dorsal cervical region and being in contact with the cheek pouch. Our investigation showed that the muscle fiber morphology was comparable in both parts. Muscle spindles were only present in regions connected to the cheek pouch and contained only nuclear chain fibers. It is tempting to speculate that they sense the filling of the cheek pouch rather than mimic activities.
Topics: Animals; Cheek; Macaca mulatta; Muscle Fibers, Skeletal; Muscle Spindles; Superficial Musculoaponeurotic System
PubMed: 34893983
DOI: 10.1111/joa.13604 -
The Journal of Physiology Nov 1981
Review
Topics: Animals; Axons; History, 19th Century; History, 20th Century; Motor Neurons; Muscle Spindles; Muscles; Neurons, Afferent; Neurons, Efferent; Neurophysiology
PubMed: 6459449
DOI: 10.1113/jphysiol.1981.sp013931 -
Journal of Neural Engineering Apr 2017We studied the fundamentals of muscle afferentation by building a Neuro-mechano-morphic system actuating a cadaveric finger. This system is a faithful implementation of...
OBJECTIVE
We studied the fundamentals of muscle afferentation by building a Neuro-mechano-morphic system actuating a cadaveric finger. This system is a faithful implementation of the stretch reflex circuitry. It allowed the systematic exploration of the effects of different fusimotor drives to the muscle spindle on the closed-loop stretch reflex response.
APPROACH
As in Part I of this work, sensory neurons conveyed proprioceptive information from muscle spindles (with static and dynamic fusimotor drive) to populations of α-motor neurons (with recruitment and rate coding properties). The motor commands were transformed into tendon forces by a Hill-type muscle model (with activation-contraction dynamics) via brushless DC motors. Two independent afferented muscles emulated the forces of flexor digitorum profundus and the extensor indicis proprius muscles, forming an antagonist pair at the metacarpophalangeal joint of a cadaveric index finger. We measured the physical response to repetitions of bi-directional ramp-and-hold rotational perturbations for 81 combinations of static and dynamic fusimotor drives, across four ramp velocities, and three levels of constant cortical drive to the α-motor neuron pool.
MAIN RESULTS
We found that this system produced responses compatible with the physiological literature. Fusimotor and cortical drives had nonlinear effects on the reflex forces. In particular, only cortical drive affected the sensitivity of reflex forces to static fusimotor drive. In contrast, both static fusimotor and cortical drives reduced the sensitivity to dynamic fusimotor drive. Interestingly, realistic signal-dependent motor noise emerged naturally in our system without having been explicitly modeled.
SIGNIFICANCE
We demonstrate that these fundamental features of spinal afferentation sufficed to produce muscle function. As such, our Neuro-mechano-morphic system is a viable platform to study the spinal mechanisms for healthy muscle function-and its pathologies such as dystonia and spasticity. In addition, it is a working prototype of a robust biomorphic controller for compliant robotic limbs and exoskeletons.
Topics: Action Potentials; Afferent Pathways; Animals; Biomimetics; Computer Simulation; Humans; Models, Neurological; Motor Neurons, Gamma; Muscle Contraction; Muscle Spindles; Muscle, Skeletal; Neuromuscular Junction; Robotics; Signal Processing, Computer-Assisted; Synaptic Transmission
PubMed: 28094764
DOI: 10.1088/1741-2552/aa59bd -
Journal of Neurophysiology Apr 2017Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the...
Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions, compliant structures can act to decouple the fascicles, and, therefore, the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1-0.5 Hz) and amplitudes (1-9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length, and spindle firing patterns. Muscle spindles are exquisitely sensitive to changes in muscle length, but recordings from human muscle spindle afferents are usually correlated with joint angle rather than muscle fascicle length. In this study, we monitored both muscle fascicle length and spindle firing from the human tibialis anterior muscle in vivo. Our findings are the first to measure these signals in vivo and provide an experimental basis for exploring this link further.
Topics: Adult; Ankle Joint; Bayes Theorem; Biophysics; Electric Stimulation; Electromyography; Female; Humans; Male; Movement; Muscle Spindles; Muscle, Skeletal; Proprioception; Tendons; Ultrasonography; Young Adult
PubMed: 28077660
DOI: 10.1152/jn.00374.2016 -
Okajimas Folia Anatomica Japonica Nov 2007We investigated the properties of the muscle spindle in the masseter muscle at an immunohistochemical level in rats fed for 6 weeks. Slow myosin heavy chain (MyHC)...
We investigated the properties of the muscle spindle in the masseter muscle at an immunohistochemical level in rats fed for 6 weeks. Slow myosin heavy chain (MyHC) isoforms were measured and intrafusal fibers in the muscle spindle were studied to determine the relationship between the superficial and deep regions of rat masseter muscle after alternated feeding pattern. However, muscle spindles were found in both regions, mainly in the deep region of the posterior superficial region of masseter muscle. The total number of the slow fiber in the intrafusal fiber and number of muscle spindle in the deep region were high from 5 to 8 weeks old in spite of various dimensions of data such as diameter and the compositions of the intrafusal fiber. The relationship of the protein expression of slow MyHC in the two regions at 5 weeks old reversed five weeks later (10 weeks old). This period is an important stage because the mastication system in masseter muscle with muscle spindle may be changed during the alternated feeding pattern of suckling to mastication. The changes may be a marker of the feeding system and of the control by the tension receptor of muscle spindle in this stage of masseter muscle after postnatal development.
Topics: Aging; Animals; Animals, Newborn; Cell Count; Cell Differentiation; Feeding Behavior; Immunohistochemistry; Male; Masseter Muscle; Mastication; Muscle Contraction; Muscle Fibers, Slow-Twitch; Muscle Spindles; Myosin Heavy Chains; Rats; Rats, Wistar; Sucking Behavior
PubMed: 18186222
DOI: 10.2535/ofaj.84.99 -
Journal of Neural Engineering Sep 2005Studies of reaching suggest that humans adapt to novel arm dynamics by building internal models that transform planned sensory states of the limb, e.g., desired limb... (Review)
Review
Studies of reaching suggest that humans adapt to novel arm dynamics by building internal models that transform planned sensory states of the limb, e.g., desired limb position and its derivatives, into motor commands, e.g., joint torques. Earlier work modeled this computation via a population of basis elements and used system identification techniques to estimate the tuning properties of the bases from the patterns of generalization. Here we hypothesized that the neural representation of planned sensory states in the internal model might resemble the signals from the peripheral sensors. These sensors normally encode the limb's actual sensory state in which movement errors occurred. We developed a set of equations based on properties of muscle spindles that estimated spindle discharge as a function of the limb's state during reaching and drawing of circles. We then implemented a simulation of a two-link arm that learned to move in various force fields using these spindle-like bases. The system produced a pattern of adaptation and generalization that accounted for a wide range of previously reported behavioral results. In particular, the bases showed gain-field interactions between encoding of limb position and velocity, very similar to the gain fields inferred from behavioral studies. The poor sensitivity of the bases to limb acceleration predicted behavioral results that were confirmed by experiment. We suggest that the internal model of limb dynamics is computed by the brain with neurons that encode the state of the limb in a manner similar to that expected of muscle spindle afferents.
Topics: Arm; Brain; Computer Simulation; Feedback; Humans; Models, Neurological; Movement; Muscle Contraction; Muscle Spindles; Muscle, Skeletal; Postural Balance; Proprioception; Reflex, Stretch
PubMed: 16135889
DOI: 10.1088/1741-2560/2/3/S09