Role of muscle spindle feedback in regulating muscle activity strength during walking at different speed in mice

Terrestrial animals increase their walking speed by increasing the activity of the extensor muscles. However, the mechanism underlying how this speed-dependent amplitude modulation is achieved remains obscure. Previous studies have shown that group Ib afferent feedback from Golgi tendon organs that signal force is one of the major regulators of the strength of muscle activity during walking in cats and humans. In contrast, the contribution of group Ia/II afferent feedback from muscle spindle stretch receptors that signal angular displacement of leg joints is unclear. Some studies indicate that group II afferent feedback may be important for amplitude regulation in humans, but the role of muscle spindle feedback in regulation of muscle activity strength in quadrupedal animals is very poorly understood. To examine the role of feedback from muscle spindles, we combined in vivo electrophysiology and motion analysis with mouse genetics and gene delivery with adeno-associated virus. We provide evidence that proprioceptive sensory feedback from muscle spindles is important for the regulation of the muscle activity strength and speed-dependent amplitude modulation. Furthermore, our data suggest that feedback from the muscle spindles of the ankle extensor muscles, the triceps surae, is the main source for this mechanism. In contrast, muscle spindle feedback from the knee extensor muscles, the quadriceps femoris, has no influence on speed-dependent amplitude modulation. We provide evidence that proprioceptive feedback from ankle extensor muscles is critical for regulating muscle activity strength as gait speed increases. NEW & NOTEWORTHY Animals upregulate the activity of extensor muscles to increase their walking speed, but the mechanism behind this is not known. We show that this speed-dependent amplitude modulation requires proprioceptive sensory feedback from muscle spindles of ankle extensor muscle. In the absence of muscle spindle feedback, animals cannot walk at higher speeds as they can when muscle spindle feedback is present.

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Steady-state response of quadriplegic subjects to inspiratory resistive load

Journal of Applied Physiology ◽

10.1152/jappl.1986.60.5.1482 ◽

1986 ◽

Vol 60 (5) ◽

pp. 1482-1492 ◽

Cited By ~ 7

Author(s):

V. Im Hof ◽

H. Dubo ◽

V. Daniels ◽

M. Younes

Keyword(s):

Steady State ◽

Chest Wall ◽

Muscle Spindles ◽

Normal Subjects ◽

Afferent Feedback ◽

Resistive Load ◽

State Response ◽

The Face ◽

Inspiratory Resistance

Normal subjects preserve tidal volume (VT) in the face of added inspiratory resistance by increasing maximal amplitude and duration of the rising phase of respiratory driving pressure (DP) and by changing the shape of this phase to one that is more concave to the time axis. To explore the possible role of chest wall afferents in mediating these responses, we determined averaged DP in eight quadriplegic subjects during steady-state unloaded breathing and while breathing through an inspiratory resistance (8.5 cmH2O X 1(-1) X s). As with normal subjects, quadriplegics preserved VT (loaded VT = 106% control) by utilizing all three mechanisms. However, prolongation of the inspiratory duration derived from the DP waveform (+22% vs. +42%) and shape response were significantly less in the quadriplegic subjects. Shape response was completely absent in subjects with C4 lesions. The results provide strong evidence that respiratory muscle spindles are responsible for shape response and that changes in afferent feedback from the chest wall play an important role in mediating inspiratory prolongation.

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The primary afferent activity cannot capture the dynamical features of muscle activity during reaching movements

10.1101/138859 ◽

2017 ◽

Author(s):

Russell L. Hardesty ◽

Matthew T. Boots ◽

Sergiy Yakovenko ◽

Valeriya Gritsenko

Keyword(s):

Muscle Activity ◽

Sensory Feedback ◽

Muscle Activation ◽

Activity Patterns ◽

Afferent Feedback ◽

Reaching Movements ◽

Afferent Activity ◽

Primary Afferent ◽

Limb Dynamics ◽

Dynamical Features

AbstractThe stabilizing role of sensory feedback in relation to realistic 3-dimensional movement dynamics remains poorly understood. The objective of this study was to quantify how primary afferent activity contributes to shaping muscle activity patterns during reaching movements. To achieve this objective, we designed a virtual reality task that guided healthy human subjects through a set of planar reaching movements with controlled kinematic and dynamic conditions that minimized inter-subject variability. Next, we integrated human upper-limb models of musculoskeletal dynamics and proprioception to analyze motion and major muscle activation patterns during these tasks. We recorded electromyographic and motion-capture data and used the integrated model to simulate joint kinematics, joint torques due to muscle contractions, muscle length changes, and simulated primary afferent feedback. The parameters of the primary afferent model were altered systematically to evaluate the effect of fusimotor drive. The experimental and simulated data were analyzed with hierarchical clustering. We found that the muscle activity patterns contained flexible task-dependent groups that consisted of co-activating agonistic and antagonistic muscles that changed with the dynamics of the task. The activity of muscles spanning only the shoulder generally grouped into a proximal cluster, while the muscles spanning the wrist grouped into a distal cluster. The bifunctional muscle spanning the shoulder and elbow were flexibly grouped with either proximal or distal cluster based on the dynamical requirements of the task. The composition and activation of these groups reflected the relative contribution of active and passive forces to each motion. In contrast, the simulated primary afferent feedback was most related to joint kinematics rather than dynamics, even though the primary afferent models had nonlinear dynamical components and variable fusimotor drive. Simulated physiological changes to the fusimotor drive were not sufficient to reproduce the dynamical features in muscle activity pattern. Altogether, these results suggest that sensory feedback signals are in a different domain from that of muscle activation signals. This indicates that to solve the neuromechanical problem, the central nervous system controls limb dynamics through task-dependent co-activation of muscles and non-linear modulation of monosynaptic primary afferent feedback.New & NoteworthyHere we answered the fundamental question in sensorimotor transformation of how primary afferent signals can contribute to the compensation for limb dynamics evident in muscle activity. We combined computational and experimental approaches to create a new experimental paradigm that challenges the nervous system with passive limb dynamics that either assists or resists the desired movement. We found that the active dynamical features present in muscle activity are unlikely to arise from direct feedback from primary afferents.

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Contribution of Sensory Feedback to the Generation of Extensor Activity During Walking in the Decerebrate Cat

Journal of Neurophysiology ◽

10.1152/jn.1999.81.2.758 ◽

1999 ◽

Vol 81 (2) ◽

pp. 758-770 ◽

Cited By ~ 110

Author(s):

Gordon W. Hiebert ◽

Keir G. Pearson

Keyword(s):

Sensory Feedback ◽

Knee Extensor ◽

Afferent Feedback ◽

Knee Extensors ◽

Total Contribution ◽

Decerebrate Cat ◽

Dorsal Roots ◽

Level Of Activity ◽

Extensor Muscles ◽

Decerebrate Cats

Contribution of sensory feedback to the generation of extensor activity during walking in the decerebrate cat. In this investigation we have estimated the afferent contribution to the generation of activity in the knee and ankle extensor muscles during walking in decerebrate cats by loading and unloading extensor muscles, and by unilateral deafferentation of a hind leg. The total contribution of afferent feedback to extensor burst generation was estimated by allowing one hind leg to step into a hole in the treadmill belt on which the animal was walking. In the absence of ground support the level of activity in knee and ankle extensor muscles was reduced to ∼70% of normal. Activity in the ankle extensors could be restored during the “foot-in-hole” trials by selectively resisting extension at the ankle. Thus feedback from proprioceptors in the ankle extensor muscles probably makes a large contribution to burst generation in these muscles during weight-bearing steps. Similarly, feedback from proprioceptors in knee extensor appears to contribute substantially to the activation of knee extensor muscles because unloading and loading these muscles, by lifting and dropping the hindquarters, strongly reduced and increased, respectively, the level of activity in the knee extensors. This conclusion was supported by the finding that partial deafferentation of one hind leg by transection of the L4–L6 dorsal roots reduced the level of activity in the knee extensors by ∼50%, but did not noticeably influence the activity in ankle extensor muscles. However, extending the deafferentation to include the L7–S2dorsal roots decreased the ankle extensor activity. We conclude that afferent feedback contributes to more than one-half of the input to knee and ankle extensor motoneurons during the stance phase of walking in decerebrate cats. The continuous contribution of afferent feedback to the generation of extensor activity could function to automatically adjust the intensity of activity to meet external demands.

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Changes in muscle spindle firing in response to length changes of neighboring muscles

Journal of Neurophysiology ◽

10.1152/jn.00937.2015 ◽

2016 ◽

Vol 115 (6) ◽

pp. 3146-3155 ◽

Cited By ~ 5

Author(s):

Hiltsje A. Smilde ◽

Jake A. Vincent ◽

Guus C. Baan ◽

Paul Nardelli ◽

Johannes C. Lodder ◽

...

Keyword(s):

Muscle Spindle ◽

Muscle Spindles ◽

Triceps Surae ◽

Connective Tissues ◽

Muscle Belly ◽

Intact Muscle ◽

Muscle Compartment ◽

Synergistic Muscles ◽

Length Changes ◽

Triceps Surae Muscles

Skeletal muscle force can be transmitted to the skeleton, not only via its tendons of origin and insertion but also through connective tissues linking the muscle belly to surrounding structures. Through such epimuscular myofascial connections, length changes of a muscle may cause length changes within an adjacent muscle and hence, affect muscle spindles. The aim of the present study was to investigate the effects of epimuscular myofascial forces on feedback from muscle spindles in triceps surae muscles of the rat. We hypothesized that within an intact muscle compartment, muscle spindles not only signal length changes of the muscle in which they are located but can also sense length changes that occur as a result of changing the length of synergistic muscles. Action potentials from single afferents were measured intra-axonally in response to ramp-hold release (RHR) stretches of an agonistic muscle at different lengths of its synergist, as well as in response to synergist RHRs. A decrease in force threshold was found for both soleus (SO) and lateral gastrocnemius afferents, along with an increase in length threshold for SO afferents. In addition, muscle spindle firing could be evoked by RHRs of the synergistic muscle. We conclude that muscle spindles not only signal length changes of the muscle in which they are located but also local length changes that occur as a result of changing the length and relative position of synergistic muscles.

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The Mammalian Muscle Spindle

Physiology ◽

10.1152/physiologyonline.1997.12.1.37 ◽

1997 ◽

Vol 12 (1) ◽

pp. 37-42 ◽

Cited By ~ 6

Author(s):

U Proske

Keyword(s):

Motor Control ◽

Muscle Spindle ◽

Muscle Spindles ◽

Mammalian Muscle ◽

Intrafusal Fibers ◽

Sensory Endings

A brief, summarizing description is given of the structure and physiology of the mammalian muscle spindle. The question is addressed, What might be the roles of the three different kinds of intrafusal fibers on which the sensory endings lie? The role of muscle spindles in proprioception and in motor control is discussed.

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Behavior of Jaw Muscle Spindle Afferents During Cortically Induced Rhythmic Jaw Movements in the Anesthetized Rabbit

Journal of Neurophysiology ◽

10.1152/jn.1999.82.5.2633 ◽

1999 ◽

Vol 82 (5) ◽

pp. 2633-2640 ◽

Cited By ~ 39

Author(s):

O. Hidaka ◽

T. Morimoto ◽

T. Kato ◽

Y. Masuda ◽

T. Inoue ◽

...

Keyword(s):

Firing Rate ◽

Muscle Spindle ◽

Muscle Activity ◽

Muscle Spindles ◽

Emg Activity ◽

Spatiotemporal Pattern ◽

Digastric Muscle ◽

Dependent Manner ◽

Jaw Movements ◽

Jaw Opening

The regulation by muscle spindles of jaw-closing muscle activity during mastication was evaluated in anesthetized rabbits. Simultaneous records were made of the discharges of muscle spindle units in the mesencephalic trigeminal nucleus, masseter and digastric muscle activity (electromyogram [EMG]), and jaw-movement parameters during cortically induced rhythmic jaw movements. One of three test strips of polyurethane foam, each of a different hardness, was inserted between the opposing molars during the jaw movements. The induced rhythmic jaw movements were crescent shaped and were divided into three phases: jaw-opening, jaw-closing, and power. The firing rate of muscle spindle units during each phase increased after strip application, with a tendency for the spindle discharge to be continuous throughout the entire chewing cycle. However, although the firing rate did not change during the jaw-opening and jaw-closing phases when the strip hardness was altered, the firing rate during the power phase increased in a hardness-dependent manner. In addition, the integrated EMG activity, the duration of the masseteric bursts, and the minimum gape increased with strip hardness. Spindle discharge during the power phase correlated with jaw-closing muscle activity, implying that the change in jaw-closing muscle activity associated with strip hardness was caused by increased spindle discharge produced through insertion of a test strip. The increased firing rate during the other two phases may be involved in a long-latency spindle feedback. This could contribute to matching the spatiotemporal pattern of the central pattern generator to that of the moving jaw.

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Increasing cutaneous afferent feedback improves proprioceptive accuracy at the knee in patients with sensory ataxia

Journal of Neurophysiology ◽

10.1152/jn.00148.2015 ◽

2016 ◽

Vol 115 (2) ◽

pp. 711-716 ◽

Cited By ~ 5

Author(s):

Vaughan G. Macefield ◽

Lucy Norcliffe-Kaufmann ◽

Niamh Goulding ◽

Jose-Alberto Palma ◽

Cristina Fuente Mora ◽

...

Keyword(s):

Correlation Coefficient ◽

Sensory Feedback ◽

Joint Angle ◽

Large Diameter ◽

Muscle Spindles ◽

Absolute Error ◽

Afferent Feedback ◽

Ataxic Gait ◽

Matching Error ◽

Matching Test

Hereditary sensory and autonomic neuropathy type III (HSAN III) features disturbed proprioception and a marked ataxic gait. We recently showed that joint angle matching error at the knee is positively correlated with the degree of ataxia. Using intraneural microelectrodes, we also documented that these patients lack functional muscle spindle afferents but have preserved large-diameter cutaneous afferents, suggesting that patients with better proprioception may be relying more on proprioceptive cues provided by tactile afferents. We tested the hypothesis that enhancing cutaneous sensory feedback by stretching the skin at the knee joint using unidirectional elasticity tape could improve proprioceptive accuracy in patients with a congenital absence of functional muscle spindles. Passive joint angle matching at the knee was used to assess proprioceptive accuracy in 25 patients with HSAN III and 9 age-matched control subjects, with and without taping. Angles of the reference and indicator knees were recorded with digital inclinometers and the absolute error, gradient, and correlation coefficient between the two sides calculated. Patients with HSAN III performed poorly on the joint angle matching test [mean matching error 8.0 ± 0.8° (±SE); controls 3.0 ± 0.3°]. Following application of tape bilaterally to the knee in an X-shaped pattern, proprioceptive performance improved significantly in the patients (mean error 5.4 ± 0.7°) but not in the controls (3.0 ± 0.2°). Across patients, but not controls, significant increases in gradient and correlation coefficient were also apparent following taping. We conclude that taping improves proprioception at the knee in HSAN III, presumably via enhanced sensory feedback from the skin.

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Treatment of vertebral fractures due to osteoporosis

Osteologie/Osteology ◽

10.1055/s-0037-1622038 ◽

2015 ◽

Vol 24 (01) ◽

pp. 7-10 ◽

Cited By ~ 3

Author(s):

M. Pfeifer ◽

M. Sinaki

Keyword(s):

Exercise Program ◽

Therapeutic Exercise ◽

Training Support ◽

Axial Stability ◽

Extensor Muscles ◽

Therapeutic Exercises ◽

Increase Risk ◽

Risk Of Falls ◽

Risk Of Fall

SummaryThe objective of exercise in the treatment of osteoporosis is to improve axial stability through strengthening of back extensor muscles. Therefore, a back extension exercise program specific to one’s musculoskeletal competence and pain can be performed in a sitting position and later advanced to the prone position. When fragility is resolved, back extension is performed against resistance applied to the upper back. A significant reduction in back pain, kyphosis, and risk of falls and an improvement in the level of physical activity have been achieved through the SPEED (Spinal Proprioceptive Extension Exercise Dynamic) program. In addition, the application of a “Posture Training Support” (PTS) using a backpack may decrease kyphosis and pain related not only to compression fractures but also reduce iliocostal friction. Therapeutic exercise should address osteo - porosis-related deformities of axial posture, which can increase risk of fall and fracture. Thus, the role of a therapeutic exercise program is to increase muscle strength safely, decrease immobility-related complications, and prevent fall and fracture. As with pharmacotherapy, therapeutic exercises are individualized.

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