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1.
Res Sq ; 2024 Jun 27.
Article in English | MEDLINE | ID: mdl-38978589

ABSTRACT

Background: Recent findings suggest increased excitatory heteronymous feedback from quadriceps onto soleus may contribute to abnormal coactivation of knee and ankle extensors after stroke. However, there is lack of consensus on whether persons post-stroke exhibit altered heteronymous reflexes and, when present, the origin of increased excitation (i.e. increased excitation alone and/or decreased inhibition). This study examined heteronymous excitation and inhibition from quadriceps onto soleus in paretic, nonparetic, and age-matched control limbs to determine whether increased excitation was due to excitatory and/or reduced inhibitory reflex circuits. A secondary purpose was to examine whether heteronymous reflex magnitudes were related to clinical measures of lower limb recovery, walking-speed, and dynamic balance. Methods: Heteronymous excitation and inhibition from quadriceps onto soleus were examined in fourteen persons post-stroke and fourteen age-matched unimpaired participants. Heteronymous feedback was elicited by femoral nerve and quadriceps muscle stimulation in separate trials while participants tonically activated soleus at 20% max. Fugl-Myer assessment of lower extremity, 10-meter walk test, and Mini-BESTest were assessed in stroke survivors. Results: Heteronymous excitation and inhibition onsets, durations, and magnitudes were not different between paretic, nonparetic or age-matched unimpaired limbs. Quadriceps stimulation elicited excitation that was half the magnitude of femoral nerve stimulation. Femoral nerve elicited paretic limb heteronymous excitation was positively correlated with walking speed but did not reach significance because only a subset of paretic limbs exhibited excitation (n = 8, Spearman r = 0.69, P = 0.058). Conclusions: Heteronymous feedback from quadriceps onto soleus assessed in a seated posture was not impaired in persons post-stroke. Despite being unable to identify whether reduced inhibition contributes to abnormal excitation reported in prior studies, our results indicate quadriceps stimulation may allow a better estimate of heteronymous inhibition in those that exhibit exaggerated excitation. Heteronymous excitation magnitude in the paretic limb was positively correlated with self-selected walking speed suggesting paretic limb excitation at the higher end of a normal range may facilitate walking ability after stroke. Future studies are needed to identify whether heteronymous feedback from Q onto SOL is altered after stroke in upright postures and during motor tasks as a necessary next step to identify mechanisms underlying motor impairment.

2.
Eur J Neurosci ; 60(3): 4317-4331, 2024 Aug.
Article in English | MEDLINE | ID: mdl-38853295

ABSTRACT

Heteronymous inhibition between lower limb muscles is primarily attributed to recurrent inhibitory circuits in humans but could also arise from Golgi tendon organs (GTOs). Distinguishing between recurrent inhibition and mechanical activation of GTOs is challenging because their heteronymous effects are both elicited by stimulation of nerves or a muscle above motor threshold. Here, the unique influence of mechanically activated GTOs was examined by comparing the magnitude of heteronymous inhibition from quadriceps (Q) muscle stimulation onto ongoing soleus electromyographic at five Q stimulation intensities (1.5-2.5× motor threshold) before and after an acute bout of stimulation-induced Q fatigue. Fatigue was used to decrease Q stimulation evoked force (i.e., decreased GTO activation) despite using the same pre-fatigue stimulation currents (i.e., same antidromic recurrent inhibition input). Thus, a decrease in heteronymous inhibition after Q fatigue and a linear relation between stimulation-evoked torque and inhibition both before and after fatigue would support mechanical activation of GTOs as a source of inhibition. A reduction in evoked torque but no change in inhibition would support recurrent inhibition. After fatigue, Q stimulation-evoked knee torque, heteronymous inhibition magnitude and inhibition duration were significantly decreased for all stimulation intensities. In addition, heteronymous inhibition magnitude was linearly related to twitch-evoked knee torque before and after fatigue. These findings support mechanical activation of GTOs as a source of heteronymous inhibition along with recurrent inhibition. The unique patterns of heteronymous inhibition before and after fatigue across participants suggest the relative contribution of GTOs, and recurrent inhibition may vary across persons.


Subject(s)
Electromyography , Muscle Fatigue , Quadriceps Muscle , Humans , Muscle Fatigue/physiology , Male , Adult , Quadriceps Muscle/physiology , Female , Muscle, Skeletal/physiology , Young Adult , Neural Inhibition/physiology , Electric Stimulation , Torque
3.
J Appl Physiol (1985) ; 136(6): 1468-1477, 2024 Jun 01.
Article in English | MEDLINE | ID: mdl-38601996

ABSTRACT

Acute exposure to hypoxia increases postural sway, but the underlying neurophysiological factors are unclear. Golgi tendon organs (GTOs), located within the musculotendinous junction (MTJ), provide inhibitory signals to plantar flexor muscles that are important for balance control; however, it is uncertain if GTO function is influenced by hypoxia. The aim of this study was to determine how normobaric hypoxia influences lower limb tendon-evoked inhibitory reflexes during upright stance. We hypothesized that tendon-evoked reflex area and duration would decrease during hypoxia, indicating less inhibition of postural muscles compared with normoxia. At baseline (BL; 0.21 fraction of inspired oxygen, FIO2) and at ∼2 (H2) and 4 (H4) h of normobaric hypoxia (0.11 FIO2) in a normobaric hypoxic chamber, 16 healthy participants received electrical musculotendinous stimulation (MTstim) to the MTJ of the left Achilles tendon. The MTstim was delivered as two sets of 50 stimuli while the participant stood on a force plate with their feet together. Tendon-evoked inhibitory reflexes were recorded from the surface electromyogram of the ipsilateral medial gastrocnemius, and center of pressure (CoP) variables were recorded from the force plate. Normobaric hypoxia increased CoP velocity (P ≤ 0.002) but not CoP standard deviation (P ≥ 0.12). Compared with BL, normobaric hypoxia reduced tendon-evoked inhibitory reflex area by 45% at H2 and 53% at H4 (P ≤ 0.002). In contrast, reflex duration was unchanged during hypoxia. The reduced inhibitory feedback from the GTO pathway could likely play a role in the increased postural sway observed during acute exposure to hypoxia.NEW & NOTEWORTHY The Ib pathway arising from the Golgi tendon organ provides inhibitory signals onto motor neuron pools that modifies force and, hence, postural control. Although hypoxia influences standing balance (increases sway), the underlying mechanisms have yet to be unraveled. Our study identified that tendon-evoked inhibition onto a plantar flexor motoneuron pool is reduced by acute exposure to normobaric hypoxia. This reduction of inhibition may contribute to the hypoxia-related increase in postural sway.


Subject(s)
Achilles Tendon , Hypoxia , Muscle, Skeletal , Reflex , Humans , Male , Hypoxia/physiopathology , Achilles Tendon/physiology , Achilles Tendon/physiopathology , Adult , Reflex/physiology , Female , Muscle, Skeletal/physiology , Young Adult , Electromyography/methods , Postural Balance/physiology , Electric Stimulation/methods
4.
Trends Genet ; 40(1): 20-23, 2024 01.
Article in English | MEDLINE | ID: mdl-37926636

ABSTRACT

Proprioception - the sense of body position in space - is intimately linked to motor control. Here, we briefly review the current knowledge of the proprioceptive system and how advances in the genetic characterisation of proprioceptive sensory neurons in mice promise to dissect its role in health and disease.


Subject(s)
Proprioception , Sensory Receptor Cells , Mice , Animals , Proprioception/physiology , Sensory Receptor Cells/physiology
5.
Exp Physiol ; 109(1): 35-44, 2024 01.
Article in English | MEDLINE | ID: mdl-37119460

ABSTRACT

Our objective was to evaluate an ex vivo muscle-nerve preparation used to study mechanosensory signalling by low threshold mechanosensory receptors (LTMRs). Specifically, we aimed to assess how well the ex vivo preparation represents in vivo firing behaviours of the three major LTMR subtypes of muscle primary sensory afferents, namely type Ia and II muscle spindle (MS) afferents and type Ib tendon organ afferents. Using published procedures for ex vivo study of LTMRs in mouse hindlimb muscles, we replicated earlier reports on afferent firing in response to conventional stretch paradigms applied to non-contracting, that is passive, muscle. Relative to in vivo studies, stretch-evoked firing for confirmed MS afferents in the ex vivo preparation was markedly reduced in firing rate and deficient in encoding dynamic features of muscle stretch. These deficiencies precluded conventional means of discriminating type Ia and II afferents. Muscle afferents, including confirmed Ib afferents were often indistinguishable based on their similar firing responses to the same physiologically relevant stretch paradigms. These observations raise uncertainty about conclusions drawn from earlier ex vivo studies that either attribute findings to specific afferent types or suggest an absence of treatment effects on dynamic firing. However, we found that replacing the recording solution with bicarbonate buffer resulted in afferent firing rates and profiles more like those seen in vivo. Improving representation of the distinctive sensory encoding properties in ex vivo muscle-nerve preparations will promote accuracy in assigning molecular markers and mechanisms to heterogeneous types of muscle mechanosensory neurons.


Subject(s)
Muscle Spindles , Tendons , Mice , Animals , Muscle Spindles/physiology , Signal Transduction , Neurons , Neurons, Afferent/physiology
6.
Trends Neurosci ; 46(12): 1083-1094, 2023 12.
Article in English | MEDLINE | ID: mdl-37858440

ABSTRACT

Proprioception, the sense of body position in space, has a critical role in the control of posture and movement. Aside from skin and joint receptors, the main sources of proprioceptive information in tetrapods are mechanoreceptive end organs in skeletal muscle: muscle spindles (MSs) and Golgi tendon organs (GTOs). The sensory neurons that innervate these receptors are divided into subtypes that detect discrete aspects of sensory information from muscles with different biomechanical functions. Despite the importance of proprioceptive neurons in motor control, the developmental mechanisms that control the acquisition of their distinct functional properties and positional identity are not yet clear. In this review, we discuss recent findings on the development of mouse proprioceptor subtypes and challenges in defining them at the molecular and functional level.


Subject(s)
Mechanoreceptors , Sensory Receptor Cells , Mice , Animals , Sensory Receptor Cells/physiology , Mechanoreceptors/physiology , Muscle Spindles/physiology , Muscle, Skeletal/innervation , Muscle, Skeletal/physiology , Proprioception/physiology
7.
Annu Rev Physiol ; 85: 1-24, 2023 02 10.
Article in English | MEDLINE | ID: mdl-36400128

ABSTRACT

The generation of an internal body model and its continuous update is essential in sensorimotor control. Although known to rely on proprioceptive sensory feedback, the underlying mechanism that transforms this sensory feedback into a dynamic body percept remains poorly understood. However, advances in the development of genetic tools for proprioceptive circuit elements, including the sensory receptors, are beginning to offer new and unprecedented leverage to dissect the central pathways responsible for proprioceptive encoding. Simultaneously, new data derived through emerging bionic neural machine-interface technologies reveal clues regarding the relative importance of kinesthetic sensory feedback and insights into the functional proprioceptive substrates that underlie natural motor behaviors.


Subject(s)
Bionics , Proprioception , Humans , Proprioception/physiology , Feedback, Sensory/physiology , Sensory Receptor Cells/physiology
8.
Exp Brain Res ; 240(9): 2375-2388, 2022 Sep.
Article in English | MEDLINE | ID: mdl-35881156

ABSTRACT

Heteronymous excitatory feedback from muscle spindles and inhibitory feedback from Golgi tendon organs and recurrent inhibitory circuits can influence motor coordination. The functional role of inhibitory feedback is difficult to determine, because nerve stimulation, the primary method used in humans, cannot evoke inhibition without first activating the largest diameter muscle spindle axons. Here, we tested the hypothesis that quadriceps muscle stimulation could be used to examine heteronymous inhibition more selectively when compared to femoral nerve stimulation by comparing the effects of nerve and muscle stimulation onto ongoing soleus EMG held at 20% of maximal effort. Motor threshold and two higher femoral nerve and quadriceps stimulus intensities matched by twitch evoked torque magnitudes were examined. We found that significantly fewer participants exhibited excitation during quadriceps muscle stimulation when compared to nerve stimulation (14-29% vs. 64-71% of participants across stimulation intensities) and the magnitude of heteronymous excitation from muscle stimulation, when present, was much reduced compared to nerve stimulation. Muscle and nerve stimulation resulted in heteronymous inhibition that significantly increased with increasing stimulation evoked torque magnitudes. This study provides novel evidence that muscle stimulation may be used to more selectively examine inhibitory heteronymous feedback between muscles in the human lower limb when compared to nerve stimulation.


Subject(s)
Femoral Nerve , Quadriceps Muscle , Electric Stimulation , Femoral Nerve/physiology , H-Reflex/physiology , Humans , Muscle Spindles/physiology , Muscle, Skeletal/physiology
9.
Exp Brain Res ; 240(1): 147-158, 2022 Jan.
Article in English | MEDLINE | ID: mdl-34677632

ABSTRACT

Skeletal muscles embed multiple tendon organs, both at the proximal and distal ends of muscle fibers. One of the functions of such spatial distribution may be to provide locally unique force feedback, which may become more important when stresses are distributed non-uniformly within the muscle. Forces exerted by connections between adjacent muscles (i.e. epimuscular myofascial forces) may cause such local differences in force. The aim of this exploratory study was to investigate the effects of mechanical interactions between adjacent muscles on sensory encoding by tendon organs. Action potentials from single afferents were recorded intra-axonally in response to ramp-hold release (RHR) stretches of a passive agonistic muscle at different lengths or relative positions of its passive synergist. The tendons of gastrocnemius (GAS), plantaris (PL) and soleus (SO) muscles were cut from the skeleton for attachment to servomotors. Connective tissues among these muscles were kept intact. Lengthening GAS + PL decreased the force threshold of SO tendon organs (p = 0.035). The force threshold of lateral gastrocnemius (LG) tendon organs was not affected by SO length (p = 0.371). Also displacing LG + PL, kept at a constant muscle-tendon unit length, from a proximal to a more distal position resulted in a decrease in force threshold of LG tendon organs (p = 0.007). These results indicate that tendon organ firing is affected by changes in length and/or relative position of adjacent synergistic muscles. We conclude that tendon organs can provide the central nervous system with information about local stresses caused by epimuscular myofascial forces.


Subject(s)
Muscle, Skeletal , Tendons , Animals , Biomechanical Phenomena , Humans , Mechanoreceptors , Muscle Contraction , Rats , Rats, Wistar
10.
Physiol Rep ; 9(8): e14834, 2021 04.
Article in English | MEDLINE | ID: mdl-33932117

ABSTRACT

This study investigated the influence of passive tension on Hoffmann reflex during the loading (muscle stretched by passive joint movement) and unloading phase (joint returned to initial position) of muscle stretching. The maximal H-reflex amplitude (Hmax ) was recorded in soleus in 19 young adults during the loading and unloading phases of a passive 30° dorsiflexion, from 90° ankle angle (reference position). Hmax was evoked at similar angles (Protocol-1) or similar passive torque (PT; Protocol-2) during the loading and unloading phases, or during two loading phases separated by a 5-min stretch hold at 30° ankle dorsiflexion relative to the reference position (Protocol-3). Homosynaptic depression (HD) was assessed with paired H reflexes (0.5-s interstimulus interval) during the loading and unloading phases (Protocol-4; n=13). In Protocol-1, PT was lesser and Hmax greater during the unloading than the loading phase (p < 0.001). In Protocol-2, no difference in Hmax was observed between phases. In Protocol-3, PT was lesser and Hmax greater during the second than the first loading phase (p < 0.001). Changes in PT during in these three protocols were associated with those in Hmax (r2  ≥ 0.97). In Protocol-4, HD increased and decreased during the loading and unloading phases, respectively (p < 0.001), without differing between phases. Additional experiments (n=12) showed a similar modulation of Hmax in gastrocnemius medialis during loading and unloading phases, while muscle fascicle length did not differ between phases. This study indicates that the H-reflex modulation during muscle stretching relies in part on mechanisms associated with the PT developed by the muscle-tendon unit.


Subject(s)
Muscle, Skeletal/physiology , Reflex, Stretch , Evoked Potentials, Motor , Female , Humans , Male , Muscle Contraction , Neural Inhibition , Synapses/physiology , Torque , Young Adult
11.
Curr Opin Physiol ; 19: 204-210, 2021 Feb.
Article in English | MEDLINE | ID: mdl-33381667

ABSTRACT

Proprioception is an essential part of motor control. The main sensory subclasses that underlie this feedback control system - muscle spindle and Golgi tendon organ afferents - have been extensively characterized at a morphological and physiological level. More recent studies are beginning to reveal the molecular foundation for distinct proprioceptor subtypes, offering new insights into their developmental ontogeny and phenotypic diversity. This review intends to highlight some of these new findings.

12.
Appl Physiol Nutr Metab ; 45(6): 601-605, 2020 Jun.
Article in English | MEDLINE | ID: mdl-31675479

ABSTRACT

Residual torque depression (rTD) is the reduction in steady-state isometric torque following an active shortening contraction when compared with an isometric contraction at the same muscle length and activation level. We have shown that spinal excitability increases in the rTD state, yet the mechanisms remains unknown. Percutaneous electrical tendon stimulation was used to induce tendon-evoked inhibitory reflexes. We demonstrated that in the rTD state, reduced torque contributes to a reduction in inhibitory afferent feedback, which indicates that the history-dependent properties of muscle can alter spinal excitability and the voluntary control of submaximal contractions through changes in peripheral afferent feedback. Novelty Residual force depression is a basic property of skeletal muscle, which can influence spinal and supraspinal excitability via inhibitory reflex activity. Residual force depression alters the voluntary control of force.


Subject(s)
Isometric Contraction/physiology , Mechanoreceptors/physiology , Tendons/physiology , Adult , Electromyography , Humans , Male , Muscle, Skeletal/physiology , Torque , Young Adult
13.
Brain Sci ; 10(1)2019 Dec 23.
Article in English | MEDLINE | ID: mdl-31878094

ABSTRACT

Residual torque enhancement (rTE) is a history-dependent property of muscle, which results in an increase in steady-state isometric torque production following an active lengthening contraction as compared to a purely isometric (ISO) contraction at the same muscle length and level of activation. Once thought to be only an intrinsic property of muscle, recent evidence during voluntary contractions indicates a neuromechanical coupling between motor neuron excitability and the contractile state of the muscle. However, the mechanism by which this occurs has yet to be elucidated. The purpose of this study was to investigate inhibition arising from tendon-mediated feedback (e.g., Golgi tendon organ; GTO) through tendon electrical stimulation (TStim) in the ISO and rTE states during activation-matching and torque-matching tasks. Fourteen male participants (22 ± 2 years) performed 10 activation-matching contractions at 40% of their maximum tibialis anterior electromyography amplitude (5 ISO/5 rTE) and 10 torque-matching contractions at 40% of their maximum dorsiflexion torque (5 ISO/5 rTE). During both tasks, 10 TStim were delivered during the isometric steady state of all contractions, and the resulting tendon-evoked inhibitory reflexes were averaged and analyzed. Reflex amplitude increased by ~23% in the rTE state compared to the ISO state for the activation-matching task, and no differences were detected for the torque-matching task. The current data indicate an important relationship between afferent feedback in the torque-enhanced state and voluntary control of submaximal contractions. The history-dependent properties of muscle is likely to alter motor neuron excitability through modifications in tension- or torque-mediated afferent feedback arising from the tendon.

14.
J Physiol ; 597(17): 4627-4642, 2019 09.
Article in English | MEDLINE | ID: mdl-31228207

ABSTRACT

KEY POINTS: Golgi tendon organ feedback has been evaluated most frequently using electrical stimulation of peripheral nerves, which is not a physiological or selective stimulus for Golgi tendon organs. Golgi tendon organs are most responsive to active muscle contractions. This study provides evidence that muscle stimulation evoked twitches - a physiological stimulus for Golgi tendon organs - induces intermuscular effects most likely due to mechanical activation of Golgi tendon organ feedback and not direct activation of sensory axons. The results demonstrate that twitch contractions are a feasible non-invasive approach that can be used to advance understanding of the functional role of Golgi tendon organ feedback. ABSTRACT: Force feedback from Golgi tendon organs (GTOs) has widespread intermuscular projections mediated by interneurons that share inputs from muscle spindles, among others. Because current methods to study GTO circuitry (nerve stimulation or muscle stretch) also activate muscle spindle afferents, the selective role of GTOs remains uncertain. Here, we tested the hypothesis that intramuscular stimulation evoked twitch contractions could be used to naturally bias activation of GTOs and thus evaluate their intermuscular effects in decerebrate cats. This was achieved by comparing the effects of twitch contractions and stretches as donor inputs onto the motor output of recipient muscles. Donor-recipient pairs evaluated included those already known in the cat to receive donor excitatory muscle spindle feedback only, inhibitory GTO feedback only, and both excitatory spindle and inhibitory GTO effects. Muscle stretch, but not twitch contractions, evoked excitation onto recipient muscles with muscle spindle afferent inputs only. Both donor muscle stretch and twitch contractions inhibited a recipient muscle with GTO projections only. In a recipient muscle that receives both muscle spindle and GTO projections, donor muscle stretch evoked both excitatory and inhibitory effects, whereas twitch contractions evoked inhibitory effects only. These data support the hypothesis that muscle stimulation evoked contractions can induce intermuscular effects most consistent with mechanical GTO receptor activation and not direct activation of sensory axons. We propose this approach can be used to evaluate GTO circuitry more selectively than muscle stretch or nerve stimulation and can be adapted to study GTO feedback non-invasively in freely moving cats and humans.


Subject(s)
Mechanoreceptors/physiology , Muscle Contraction/physiology , Animals , Axons/physiology , Cats , Electric Stimulation/methods , Feedback , Muscle Spindles/physiology , Muscle, Skeletal/physiology , Sensory Receptor Cells/physiology
15.
J Neurosci ; 39(22): 4252-4267, 2019 05 29.
Article in English | MEDLINE | ID: mdl-30926747

ABSTRACT

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 organ-derived signals.SIGNIFICANCE STATEMENT 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 organ-derived signals.


Subject(s)
Feedback, Sensory/physiology , Mechanoreceptors/physiology , Muscle Spindles/physiology , Proprioception/physiology , Animals , Female , Male , Membrane Proteins/metabolism , Mice , Muscle Spindles/innervation , Phenotype
16.
Exp Brain Res ; 237(3): 589-599, 2019 Mar.
Article in English | MEDLINE | ID: mdl-30604022

ABSTRACT

Effort, force and heaviness are related terms, having in common that they are all sensations associated with the generation of voluntary muscle contractions. Traditionally they have been thought to originate in the brain, as a result of copies of motor commands relayed to sensory areas. A stumbling block for the central hypothesis has been the lack of proportionality between the fall in muscle force from fatigue or paralysis and the increase in sensation generated while trying to achieve the required force. In recent times growing evidence has accumulated supporting a role for peripheral sensory receptors, in particular the muscle spindles, as contributing to these sensations. The review discusses the evidence for participation of sensory receptors and what this means for proprioception. In particular, it is not straightforward to envisage how muscle spindles might provide a reliable force signal in a contracting muscle, with or without support from the fusimotor system. An important additional consideration is the method of measurement. It has emerged that there is evidence of a task-dependency in the composition of the afferent signals contributing to the sense of force. The evidence suggests that the signal used in a two-arm force matching task is not the same as in a one-arm task. It will be important, in the future, to try and obtain more direct evidence about the afferent origins of the senses of effort, force and heaviness, how they might change from one task to another and what implications this has for motor control.


Subject(s)
Motor Activity/physiology , Muscle Contraction/physiology , Muscle Spindles/physiology , Perception/physiology , Proprioception/physiology , Sensation/physiology , Humans
17.
J Neurosci ; 38(16): 3929-3938, 2018 04 18.
Article in English | MEDLINE | ID: mdl-29563182

ABSTRACT

Noninvasive assessment of spinal circuitry in humans is limited, especially for Ib pathways in the upper limb. We developed a protocol in which we evoke the H-reflex in flexor carpi radialis (FCR) by median nerve stimulation and condition it with electrical stimulation above motor threshold over the extensor carpi radialis (ECR) muscle belly. Eighteen healthy adults (8 male, 10 female) took part in the study. There was a clear reflex facilitation at a 30 ms interstimulus interval (ISI) and suppression at a 70 ms ISI, which was highly consistent across subjects. We investigated the following two hypotheses of the possible source of the facilitation: (1) ECR Ib afferents from Golgi tendon organs, activated by the twitch following ECR stimulation; and (2) FCR afferents, from spindles and/or Golgi tendon organs, activated by the wrist extension movement that follows ECR stimulation. Several human and monkey experiments indicated a role for both of these sets of afferents. Our results provide evidence for a spinal circuit in which flexor motoneurons receive convergent excitatory input from flexor afferents as well as from extensor Ib afferents; this circuit can be straightforwardly assessed noninvasively in humans.SIGNIFICANCE STATEMENT Here we described a novel spinal circuit, which is easy to assess noninvasively in humans. Understanding this circuit in more detail could be beneficial for the design of clinical tests in neurological conditions.


Subject(s)
Median Nerve/physiology , Muscle, Skeletal/physiology , Spinal Cord/physiology , Wrist/physiology , Adolescent , Adult , Animals , Female , H-Reflex , Humans , Macaca mulatta , Male , Mechanoreceptors/physiology , Middle Aged , Motor Neurons/physiology , Muscle, Skeletal/innervation , Wrist/innervation
18.
J Neurophysiol ; 119(2): 668-678, 2018 02 01.
Article in English | MEDLINE | ID: mdl-29142095

ABSTRACT

Prior work has suggested that Golgi tendon organ feedback, via its distributed network linking muscles spanning all joints, could be used by the nervous system to help regulate whole limb mechanics if appropriately organized. We tested this hypothesis by characterizing the patterns of intermuscular force-dependent feedback between the primary extensor muscles spanning the knee, ankle, and toes in decerebrate cat hindlimbs. Intermuscular force feedback was evaluated by stretching tendons of selected muscles in isolation and in pairwise combinations and then measuring the resulting force-dependent intermuscular interactions. The relative inhibitory feedback between extensor muscles was examined, as well as symmetry of the interactions across limbs. Differences in the directional biases of inhibitory feedback were observed across cats, with three patterns identified as points on a spectrum: pattern 1, directional bias of inhibitory feedback onto the ankle extensors and toe flexors; pattern 2, convergence of inhibitory feedback onto ankle extensors and mostly balanced inhibitory feedback between vastus muscle group and flexor hallucis longus, and pattern 3, directional bias of inhibitory feedback onto ankle and knee extensors. The patterns of inhibitory feedback, while different across cats, were symmetric across limbs of individual cats. The variable but structured distribution of force feedback across cat hindlimbs provides preliminary evidence that inhibitory force feedback could be a regulated neural control variable. We propose the directional biases of inhibitory feedback observed experimentally could provide important task-dependent benefits, such as directionally appropriate joint compliance, joint coupling, and compensation for nonuniform inertia. NEW & NOTEWORTHY Feedback from Golgi tendon organs project widely among extensor motor nuclei in the spinal cord. The distributed nature of force feedback suggests these pathways contribute to the global regulation of limb mechanics. Analysis of this network in individual animals indicates that the strengths of these pathways can be reorganized appropriately for a variety of motor tasks, including level walking, slope walking, and landing.


Subject(s)
Feedback, Physiological , Hindlimb/physiology , Muscle, Skeletal/physiology , Neural Inhibition , Animals , Biomechanical Phenomena , Cats , Female , Hindlimb/innervation , Mechanoreceptors/physiology , Spinal Cord/physiology
19.
J Athl Train ; 52(10): 918-924, 2017 Oct.
Article in English | MEDLINE | ID: mdl-28796528

ABSTRACT

CONTEXT: Exercise-associated muscle cramps are a common clinical problem for athletes. OBJECTIVE: To determine whether acute passive static stretching altered cramp threshold frequency (CTF) of electrically induced muscle cramps. DESIGN: Crossover study. SETTING: Laboratory. PATIENTS OR OTHER PARTICIPANTS: Seventeen healthy college-aged individuals. INTERVENTION(S): Stretching or no stretching. MAIN OUTCOME MEASURE(S): The independent variable was the static stretch versus the no-stretch condition, and the dependent variable was the CTF. RESULTS: The CTF increased in both the control (pretest: 18.12 ± 6.46 Hz, posttest: 19.65 ± 7.25 Hz; P = .033) and stretching (pretest: 18.94 ± 5.96 Hz, posttest: 20.47 ± 7.12 Hz; P = .049) groups. No difference between the groups was found (t15 = 0.035, P = .97). CONCLUSIONS: Acute passive static stretching did not seem to increase the CTF.


Subject(s)
Muscle Contraction/physiology , Muscle Cramp/prevention & control , Muscle Stretching Exercises/methods , Muscle, Skeletal/physiology , Adult , Cross-Over Studies , Female , Humans , Male , Mechanoreceptors/physiology , Muscle Cramp/physiopathology
20.
Dev Cell ; 42(4): 388-399.e3, 2017 08 21.
Article in English | MEDLINE | ID: mdl-28829946

ABSTRACT

Maintaining posture requires tight regulation of the position and orientation of numerous spinal components. Yet, surprisingly little is known about this regulatory mechanism, whose failure may result in spinal deformity as in adolescent idiopathic scoliosis. Here, we use genetic mouse models to demonstrate the involvement of proprioception in regulating spine alignment. Null mutants for Runx3 transcription factor, which lack TrkC neurons connecting between proprioceptive mechanoreceptors and spinal cord, developed peripubertal scoliosis not preceded by vertebral dysplasia or muscle asymmetry. Deletion of Runx3 in the peripheral nervous system or specifically in peripheral sensory neurons, or of enhancer elements driving Runx3 expression in proprioceptive neurons, induced a similar phenotype. Egr3 knockout mice, lacking muscle spindles, but not Golgi tendon organs, displayed a less severe phenotype, suggesting that both receptor types may be required for this regulatory mechanism. These findings uncover a central role for the proprioceptive system in maintaining spinal alignment.


Subject(s)
Core Binding Factor Alpha 3 Subunit/genetics , Early Growth Response Protein 3/genetics , Mechanoreceptors/metabolism , Proprioception , Scoliosis/genetics , Animals , Enhancer Elements, Genetic , Mechanoreceptors/physiology , Mice , Mice, Inbred C57BL , Muscle, Skeletal/growth & development , Muscle, Skeletal/metabolism , Muscle, Skeletal/physiology , Phenotype , Spinal Cord/growth & development , Spinal Cord/metabolism , Spinal Cord/physiology
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