Functional properties of human muscle spindles

Macefield, Vaughan G.; Knellwolf, Thomas P.

doi:10.1152/jn.00071.2018

Cited by 121 publications

(96 citation statements)

References 154 publications

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“…Second, trimethaphan‐resistant APs were unlikely to represent Type I/II proprioceptive fibre activity, as the myelination of these nerves produces wider APs with prominent positive‐going depolarization (Vallbo et al . ; Macefield & Knellwolf, ), which are distinct from the sympathetic C‐fibre APs detected by the wavelet model used here (Salmanpour et al . ).…”

Section: Discussionmentioning

confidence: 50%

The role of the paravertebral ganglia in human sympathetic neural discharge patterns

Klassen

Limberg

Baker

et al. 2018

The Journal of Physiology

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Do the ganglia contribute to the ordered behaviour of postganglionic neuronal discharge within the sympathetic nervous system? To further understand the functional organization of the sympathetic nervous system we employed the microneurographic approach to record muscle sympathetic nerve activity (MSNA) and a continuous wavelet transform to study postganglionic action potential (AP) behaviour during nicotinic blockade at the ganglia (trimethaphan camsylate, 1-7 mg min ) in seven females (37 ± 5 years). Trimethaphan elicited a progressive reduction in sympathetic outflow characterized by fewer integrated bursts with decaying amplitude. Underlying trimethaphan-mediated attenuations in integrated MSNA were reductions in AP incidence (186 ± 101 to 29 ± 31 AP (100 beats) ) and AP content per integrated burst (7 ± 2 to 3 ± 1 APs burst ) (both P < 0.01) in the final minute of detectable bursting activity in the trimethaphan condition, compared to baseline. We observed an ordered de-recruitment of larger to smaller AP clusters active at baseline (14 ± 3 to 8 ± 2 active AP clusters, P < 0.01). Following cessation of integrated bursts in the trimethaphan condition, the smallest 6 ± 2 sympathetic AP clusters persisted to fire in an asynchronous pattern (49 ± 41 AP (100 beats) ) in all participants. Valsalva's manoeuvre did not increase the incidence of these persistent APs (60 ± 42 AP (100 beats) , P = 0.52), or recruit any larger APs in six of seven participants (6 ± 1 total AP clusters, P = 0.30). These data suggest that the ganglia participate in the ordered recruitment of differently sized postganglionic sympathetic nerves.

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Section: Discussionmentioning

confidence: 50%

The role of the paravertebral ganglia in human sympathetic neural discharge patterns

Klassen

Limberg

Baker

et al. 2018

The Journal of Physiology

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“…Muscle afferent proprioceptive sensory neurons (pSNs), which provide a large component of this feedback, reside in Dorsal Root Ganglia (DRG) and innervate one of two distinct receptor organs in muscle: muscle spindles (MSs) or Golgi tendon organs (GTOs) (Matthews, 1972;Windhorst, 2007). MSs are innervated by Group Ia and Group II afferents and relay the rate and magnitude of changes in muscle length, respectively (Hunt, 1990;Macefield and Knellwolf, 2018). GTOs, in contrast, are innervated by Group Ib afferents and provide information on muscle tension (Houk and Henneman, 1967;Jami, 1992).…”

Section: Introductionmentioning

confidence: 99%

A Role for Sensory end Organ-Derived Signals in Regulating Muscle Spindle Proprioceptor Phenotype

Schieren

Qian

et al. 2019

J. Neurosci.

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Proprioceptive feedback from Group Ia/II muscle spindle afferents and Group Ib Golgi tendon afferents is critical for the normal execution of most motor tasks, yet how these distinct proprioceptor subtypes emerge during development remains poorly understood. Using molecular genetic approaches in mice of either sex, we identified 24 transcripts that have not previously been associated with a proprioceptor identity. Combinatorial expression analyses of these markers reveal at least three molecularly distinct proprioceptor subtypes. In addition, we find that 12 of these transcripts are expressed well after proprioceptors innervate their respective sensory receptors, and expression of three of these markers, including the heart development molecule Heg1, is significantly reduced in mice that lack muscle spindles. These data reveal Heg1 as a putative marker for proprioceptive muscle spindle afferents. Moreover, they suggest that the phenotypic specialization of functionally distinct proprioceptor subtypes depends, in part, on extrinsic sensory receptor organderived signals. Sensory feedback from muscle spindle (MS) and Golgi tendon organ (GTO) sensory end organs is critical for normal motor control, but how distinct MS and GTO afferent sensory neurons emerge during development remains poorly understood. Using (bulk)transcriptome analysis of genetically identified proprioceptors, this work reveals molecular markers for distinct proprioceptor subsets, including some that appear selectively expressed in MS afferents. Detailed analysis of the expression of these transcripts provides evidence that MS/GTO afferent subtype phenotypes may, at least in part, emerge through extrinsic, sensory end organderived signals.

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“…During movement, the dynamic fusimotor action changes mainly the velocity sensitivity of the Ia afferents, while the static fusimotor action changes mainly the length sensitivity of the Ia afferents 21,22 . How exactly the activity of γ motoneurons changes during reaching movements in humans is unknown (for the reviews of afferent recording studies see 22,23 ). However, the effect the fusimotor drive has on shaping the muscle spindle output can be broadly classified based on whether the fusimotor drive is constant or changing during movement.…”

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confidence: 99%

Computational evidence for nonlinear feedforward modulation of fusimotor drive to antagonistic co-contracting muscles

Hardesty

Boots

Yakovenko

et al. 2020

Sci Rep

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the sensorimotor integration during unconstrained reaching movements in the presence of variable environmental forces remains poorly understood. the objective of this study was to quantify how much the primary afferent activity of muscle spindles can contribute to shaping muscle coactivation patterns during reaching movements with complex dynamics. to achieve this objective, we designed a virtual reality task that guided healthy human participants through a set of planar reaching movements with controlled kinematic and dynamic conditions that were accompanied by variable muscle co-contraction. Next, we approximated the Ia afferent activity using a phenomenological model of the muscle spindle and muscle lengths derived from a musculoskeletal model. the parameters of the spindle model were altered systematically to evaluate the effect of fusimotor drive on the shape of the temporal profile of afferent activity during movement. The experimental and simulated data were analyzed with hierarchical clustering. We found that the pattern of co-activation of agonistic and antagonistic muscles changed based on whether passive forces in each movement played assistive or resistive roles in limb dynamics. the reaching task with assistive limb dynamics was associated with the most muscle co-contraction. In contrast, the simulated Ia afferent profiles were not changing between tasks and they were largely reciprocal with homonymous muscle activity. Simulated physiological changes to the fusimotor drive were not sufficient to reproduce muscle co-contraction. These results largely rule out the static set and α-γ coactivation as the main types of fusimotor drive that transform the monosynaptic Ia afferent feedback into task-dependent co-contraction of antagonistic muscles. We speculate that another type of nonlinear transformation of Ia afferent signals that is independent of signals modulating the activity of α motoneurons is required for Ia afferent-based co-contraction. This transformation could either be applied through a complex nonlinear profile of fusimotor drive that is not yet experimentally observed or through presynaptic inhibition. Movement is the product of interactions between neural signals and the musculoskeletal dynamics that depends on limb anatomy 1-4. The motor control problem is then solved within a system with coupled neural and mechanical dynamical elements 5-7. Therefore, the relationship between neural signals driving muscle contraction and the resulting motion is nonlinear. Muscle contractions generate forces that sum into active moments defined by the agonistic or antagonistic relationships between the muscle's moment arms around a given axis of rotation of the joint. The components of these forces that sum to zero moment, such as forces produced by balanced

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Functional properties of human muscle spindles

Cited by 121 publications

References 154 publications

The role of the paravertebral ganglia in human sympathetic neural discharge patterns

The role of the paravertebral ganglia in human sympathetic neural discharge patterns

A Role for Sensory end Organ-Derived Signals in Regulating Muscle Spindle Proprioceptor Phenotype

Computational evidence for nonlinear feedforward modulation of fusimotor drive to antagonistic co-contracting muscles

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