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Assessment of Homonymous Recurrent Inhibition during Voluntary Contraction by Conditioning Nerve Stimulation

View Article: PubMed Central - PubMed

ABSTRACT

In humans, the amount of spinal homonymous recurrent inhibition during voluntary contraction is usually assessed by using a peripheral nerve stimulation paradigm. This method consists of conditioning the maximal M-wave (SM stimulus) with prior reflex stimulation (S1), with 10 ms inter-stimulus interval (ISI). The decrease observed between unconditioned (S1 only) and conditioned (S1+SM) reflex size is then attributed to recurrent inhibition. However, during a voluntary contraction, a superimposed SM stimulation leads to a maximal M-wave followed by a voluntary (V) wave at similar latency than the H-reflex. This wave can therefore interfere with the conditioned H-reflex when two different stimulation intensities are used (S1 and SM), leading to misinterpretation of the data. The aim of the present study was to assess if conditioning V-wave response instead of H-reflex, by applying SM for both stimuli (test and conditioning), can be used as an index of recurrent inhibition. Conditioned and unconditioned responses of soleus and medial gastrocnemius muscles were recorded in twelve subjects at 25% and at 50% of maximal voluntary contraction at the usual ISI of 10 ms and an optimal inter-stimulus of 15 ms determined upon M- and V-wave latencies. Conditioned H-reflex (obtained with S1+SM paradigm) was significantly lower than the unconditioned by ~30% on average, meaning that the amount of inhibition was 70%. This amount of recurrent inhibition was significantly lower at higher force level with both methods. Regardless of the level of force or the conditioning ISI, results obtained with V-wave conditioning (SM+SM) were similar at both force levels, linearly correlated and proportional to those obtained with H conditioning. Then, V-wave conditioning appears to be a reliable index of homonymous recurrent inhibition during voluntary contraction.

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Related in: MedlinePlus

Illustration of the usual method to elicit conditioned H’ reflex response.The method consisting of evoking two stimuli over the peripheral nerve is described at rest (A) and during voluntary contraction (B). Each panel represents an EMG trace of the corresponding response (left) and a schema of the spinal circuitry (right) in which arrows represent the different volleys elicited directly on motor axons (black arrows), reflexively (white arrows) or by voluntary neural drive (grey arrows). Two alpha motoneurons are represented (X and Y) and are noted with an asterisk when they are activated. It can be noticed that both motoneurons activate a Renshaw inhibitory interneuron, noted R. A) 1. the response to single S1 stimulus is depicted: the stimulation of the peripheral nerve induced a depolarization of a certain proportion of Ia afferents and thus lead to activate motoneuron X to induce a single H1 reflex response. 2. the response to single SM stimulus is depicted: this stimulation will induce a depolarization of all afferents (Ia) and efferent fibres (motor axons). On one hand, the direct activation of all motor axons towards the muscle leads to a maximal M-wave (Mmax). On the other hand, the antidromic volley towards the spinal cord will collide with reflexive activation of all motoneurons (X and Y). 3. Combined conditioning (S1) and test (SM) stimulation at 10 ms intervals. At 2 ms after SM, the H1 reflex discharge of X motoneuron (white arrow) collides with the antidromic impulse from SM in X axon. 8 ms after SM, both motoneurones (X and Y) are activated by the Ia afferent volley elicited by the SM test stimulus: a reflex response develops in both motoneurones X and Y. However, this response is blocked in motoneurone Y due to antidromic collision but not in motoneurone X in which the collision already occurred with H1 reflex response. If H’ < H1: activation of inhibitory renshaw cell by prior S1 effect. B) The example of a submaximal voluntary contraction is depicted. Thus, only X motoneurons is activated by descending command. 1. The production of H1 response is similar to rest. 2. However, single SM stimulus during voluntary contraction induced a reflexive response (V1) because the antidromic collision occurred in X axon with descending volley (grey arrow), allowing the reflexive response from SM to reach the muscle. 3. During voluntary contraction, the mechanisms inducing H’ is rather difficult to interpret because of a confounding effect of the several inputs to the motoneurons from S1, SM and the descending volley. Particularly, the influence of V1 over H’ is not elucidated.
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pone.0167062.g001: Illustration of the usual method to elicit conditioned H’ reflex response.The method consisting of evoking two stimuli over the peripheral nerve is described at rest (A) and during voluntary contraction (B). Each panel represents an EMG trace of the corresponding response (left) and a schema of the spinal circuitry (right) in which arrows represent the different volleys elicited directly on motor axons (black arrows), reflexively (white arrows) or by voluntary neural drive (grey arrows). Two alpha motoneurons are represented (X and Y) and are noted with an asterisk when they are activated. It can be noticed that both motoneurons activate a Renshaw inhibitory interneuron, noted R. A) 1. the response to single S1 stimulus is depicted: the stimulation of the peripheral nerve induced a depolarization of a certain proportion of Ia afferents and thus lead to activate motoneuron X to induce a single H1 reflex response. 2. the response to single SM stimulus is depicted: this stimulation will induce a depolarization of all afferents (Ia) and efferent fibres (motor axons). On one hand, the direct activation of all motor axons towards the muscle leads to a maximal M-wave (Mmax). On the other hand, the antidromic volley towards the spinal cord will collide with reflexive activation of all motoneurons (X and Y). 3. Combined conditioning (S1) and test (SM) stimulation at 10 ms intervals. At 2 ms after SM, the H1 reflex discharge of X motoneuron (white arrow) collides with the antidromic impulse from SM in X axon. 8 ms after SM, both motoneurones (X and Y) are activated by the Ia afferent volley elicited by the SM test stimulus: a reflex response develops in both motoneurones X and Y. However, this response is blocked in motoneurone Y due to antidromic collision but not in motoneurone X in which the collision already occurred with H1 reflex response. If H’ < H1: activation of inhibitory renshaw cell by prior S1 effect. B) The example of a submaximal voluntary contraction is depicted. Thus, only X motoneurons is activated by descending command. 1. The production of H1 response is similar to rest. 2. However, single SM stimulus during voluntary contraction induced a reflexive response (V1) because the antidromic collision occurred in X axon with descending volley (grey arrow), allowing the reflexive response from SM to reach the muscle. 3. During voluntary contraction, the mechanisms inducing H’ is rather difficult to interpret because of a confounding effect of the several inputs to the motoneurons from S1, SM and the descending volley. Particularly, the influence of V1 over H’ is not elucidated.

Mentions: The method commonly used in humans to assess homonymous recurrent inhibition consists of delivering two electrical stimuli at short interstimulus interval (ISI) over the mixed peripheral nerve [7–9]. Fig 1 depicts a summary of the method. The first stimulus (S1) provides a prior reflexive activation of the motoneuronal pool via Ia afferent depolarization while the second is evoked at maximal intensity (SM) and recruits all axons available in the nerve, i.e. eliciting a maximal M-wave, Mmax (Fig 1.1 and 1.2). With an appropriate ISI, the antidromic volley generated by SM will collide with the S1 reflexive volley in motoneuronal axons. Thus, the afferent activation of motoneuronal pool by SM, normally cancelled by the motor axonal antidromic volley, is allowed to reach the muscle again in the axons for which the collision between SM and S1 has occurred (Fig 1.3). The decrease observed between unconditioned H-reflex (S1 only) and conditioned response (S1+SM) called H', was then mainly attributed to recurrent inhibition [7,8], despite the fact that other mechanisms such as after-hyper-polarization or Golgi inhibitory circuit mediated by Ib afferents can also be involved, at least until 10ms after the first stimulus [10].


Assessment of Homonymous Recurrent Inhibition during Voluntary Contraction by Conditioning Nerve Stimulation
Illustration of the usual method to elicit conditioned H’ reflex response.The method consisting of evoking two stimuli over the peripheral nerve is described at rest (A) and during voluntary contraction (B). Each panel represents an EMG trace of the corresponding response (left) and a schema of the spinal circuitry (right) in which arrows represent the different volleys elicited directly on motor axons (black arrows), reflexively (white arrows) or by voluntary neural drive (grey arrows). Two alpha motoneurons are represented (X and Y) and are noted with an asterisk when they are activated. It can be noticed that both motoneurons activate a Renshaw inhibitory interneuron, noted R. A) 1. the response to single S1 stimulus is depicted: the stimulation of the peripheral nerve induced a depolarization of a certain proportion of Ia afferents and thus lead to activate motoneuron X to induce a single H1 reflex response. 2. the response to single SM stimulus is depicted: this stimulation will induce a depolarization of all afferents (Ia) and efferent fibres (motor axons). On one hand, the direct activation of all motor axons towards the muscle leads to a maximal M-wave (Mmax). On the other hand, the antidromic volley towards the spinal cord will collide with reflexive activation of all motoneurons (X and Y). 3. Combined conditioning (S1) and test (SM) stimulation at 10 ms intervals. At 2 ms after SM, the H1 reflex discharge of X motoneuron (white arrow) collides with the antidromic impulse from SM in X axon. 8 ms after SM, both motoneurones (X and Y) are activated by the Ia afferent volley elicited by the SM test stimulus: a reflex response develops in both motoneurones X and Y. However, this response is blocked in motoneurone Y due to antidromic collision but not in motoneurone X in which the collision already occurred with H1 reflex response. If H’ < H1: activation of inhibitory renshaw cell by prior S1 effect. B) The example of a submaximal voluntary contraction is depicted. Thus, only X motoneurons is activated by descending command. 1. The production of H1 response is similar to rest. 2. However, single SM stimulus during voluntary contraction induced a reflexive response (V1) because the antidromic collision occurred in X axon with descending volley (grey arrow), allowing the reflexive response from SM to reach the muscle. 3. During voluntary contraction, the mechanisms inducing H’ is rather difficult to interpret because of a confounding effect of the several inputs to the motoneurons from S1, SM and the descending volley. Particularly, the influence of V1 over H’ is not elucidated.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5120836&req=5

pone.0167062.g001: Illustration of the usual method to elicit conditioned H’ reflex response.The method consisting of evoking two stimuli over the peripheral nerve is described at rest (A) and during voluntary contraction (B). Each panel represents an EMG trace of the corresponding response (left) and a schema of the spinal circuitry (right) in which arrows represent the different volleys elicited directly on motor axons (black arrows), reflexively (white arrows) or by voluntary neural drive (grey arrows). Two alpha motoneurons are represented (X and Y) and are noted with an asterisk when they are activated. It can be noticed that both motoneurons activate a Renshaw inhibitory interneuron, noted R. A) 1. the response to single S1 stimulus is depicted: the stimulation of the peripheral nerve induced a depolarization of a certain proportion of Ia afferents and thus lead to activate motoneuron X to induce a single H1 reflex response. 2. the response to single SM stimulus is depicted: this stimulation will induce a depolarization of all afferents (Ia) and efferent fibres (motor axons). On one hand, the direct activation of all motor axons towards the muscle leads to a maximal M-wave (Mmax). On the other hand, the antidromic volley towards the spinal cord will collide with reflexive activation of all motoneurons (X and Y). 3. Combined conditioning (S1) and test (SM) stimulation at 10 ms intervals. At 2 ms after SM, the H1 reflex discharge of X motoneuron (white arrow) collides with the antidromic impulse from SM in X axon. 8 ms after SM, both motoneurones (X and Y) are activated by the Ia afferent volley elicited by the SM test stimulus: a reflex response develops in both motoneurones X and Y. However, this response is blocked in motoneurone Y due to antidromic collision but not in motoneurone X in which the collision already occurred with H1 reflex response. If H’ < H1: activation of inhibitory renshaw cell by prior S1 effect. B) The example of a submaximal voluntary contraction is depicted. Thus, only X motoneurons is activated by descending command. 1. The production of H1 response is similar to rest. 2. However, single SM stimulus during voluntary contraction induced a reflexive response (V1) because the antidromic collision occurred in X axon with descending volley (grey arrow), allowing the reflexive response from SM to reach the muscle. 3. During voluntary contraction, the mechanisms inducing H’ is rather difficult to interpret because of a confounding effect of the several inputs to the motoneurons from S1, SM and the descending volley. Particularly, the influence of V1 over H’ is not elucidated.
Mentions: The method commonly used in humans to assess homonymous recurrent inhibition consists of delivering two electrical stimuli at short interstimulus interval (ISI) over the mixed peripheral nerve [7–9]. Fig 1 depicts a summary of the method. The first stimulus (S1) provides a prior reflexive activation of the motoneuronal pool via Ia afferent depolarization while the second is evoked at maximal intensity (SM) and recruits all axons available in the nerve, i.e. eliciting a maximal M-wave, Mmax (Fig 1.1 and 1.2). With an appropriate ISI, the antidromic volley generated by SM will collide with the S1 reflexive volley in motoneuronal axons. Thus, the afferent activation of motoneuronal pool by SM, normally cancelled by the motor axonal antidromic volley, is allowed to reach the muscle again in the axons for which the collision between SM and S1 has occurred (Fig 1.3). The decrease observed between unconditioned H-reflex (S1 only) and conditioned response (S1+SM) called H', was then mainly attributed to recurrent inhibition [7,8], despite the fact that other mechanisms such as after-hyper-polarization or Golgi inhibitory circuit mediated by Ib afferents can also be involved, at least until 10ms after the first stimulus [10].

View Article: PubMed Central - PubMed

ABSTRACT

In humans, the amount of spinal homonymous recurrent inhibition during voluntary contraction is usually assessed by using a peripheral nerve stimulation paradigm. This method consists of conditioning the maximal M-wave (SM stimulus) with prior reflex stimulation (S1), with 10 ms inter-stimulus interval (ISI). The decrease observed between unconditioned (S1 only) and conditioned (S1+SM) reflex size is then attributed to recurrent inhibition. However, during a voluntary contraction, a superimposed SM stimulation leads to a maximal M-wave followed by a voluntary (V) wave at similar latency than the H-reflex. This wave can therefore interfere with the conditioned H-reflex when two different stimulation intensities are used (S1 and SM), leading to misinterpretation of the data. The aim of the present study was to assess if conditioning V-wave response instead of H-reflex, by applying SM for both stimuli (test and conditioning), can be used as an index of recurrent inhibition. Conditioned and unconditioned responses of soleus and medial gastrocnemius muscles were recorded in twelve subjects at 25% and at 50% of maximal voluntary contraction at the usual ISI of 10 ms and an optimal inter-stimulus of 15 ms determined upon M- and V-wave latencies. Conditioned H-reflex (obtained with S1+SM paradigm) was significantly lower than the unconditioned by ~30% on average, meaning that the amount of inhibition was 70%. This amount of recurrent inhibition was significantly lower at higher force level with both methods. Regardless of the level of force or the conditioning ISI, results obtained with V-wave conditioning (SM+SM) were similar at both force levels, linearly correlated and proportional to those obtained with H conditioning. Then, V-wave conditioning appears to be a reliable index of homonymous recurrent inhibition during voluntary contraction.

No MeSH data available.


Related in: MedlinePlus