Recurrent inhibition of firing motoneurones in man

doi:10.1016/0013-4694(88)90213-1

Electroencephalography and Clinical Neurophysiology

Volume 69, Issue 2, February 1988, Pages 179-185

https://doi.org/10.1016/0013-4694(88)90213-1 Get rights and content

Abstract

The effects of antidromic stimulation of large motoneurones on firing small motoneurones of soleus muscle have been studied. Against the background of rhythmic firing of small motor units (MUs) activated during weak voluntary muscle contraction, thick efferents of the tibialis posterior nerve were selectively stimulated and an M response was evoked in which small MUs were not involved. This provided a means of avoiding antidromic stimulation of the motoneurone under study and, thus, analysing the effect of stimulation without its summation with after-hyperpolarization. The background firing rate of MUs was 4.5–9.2/sec. PSTHs revealed a distinct inhibitory effect with a latency of 35–40 msec (slightly exceeding the latency of monosynaptic reflex) and duration 5–30 msec. It was concluded that the short-latency inhibition could be identified as recurrent inhibition. The effectiveness of recurrent inhibition evaluated by the lengthening of the interspike interval was shown to depend on the arrival time of the volley in the interval and on the background firing rate of the motoneurone. When the inhibitory volley arrived at the beginning of the interspike interval it was ineffective. This indicates that in the investigated range of firing rates the motoneurone is unable to exert an inhibitory effect on its own firing via recurrent collaterals. The inhibitory volley became highly effective at the end of an interspike interval, when the membrane potential approached threshold. The lengthening of interspike interval was more marked at a lower firing rate of the motoneurone. An increase in the background firing rate reduced the extent of recurrent inhibition (at a rate above 10/sec up to its complete ineffectiveness). Various methods for evaluating recurrent inhibition in a firing motoneurone are compared.

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Cited by (32)

Amyotrophic lateral sclerosis weakens spinal recurrent inhibition and post-activation depression
2020, Clinical Neurophysiology
Citation Excerpt :
To study RI, we stimulated the largest diameter motor axons without evoking the H-reflex in the tibial nerve while recording from the smaller motor units. Stimulation of the motor axons antidromically activates motoneuron cell body and orthodromically activates Renshaw cells via axon collaterals which in turn inhibits firing motoneurons (Kudina and Pantseva, 1988; Özyurt et al., 2019). There is also a chance that an F-wave may also activate Renshaw cells orthodromically.
Amyotrophic lateral sclerosis (ALS) disrupts motoneurons that control movement and some vital functions, however, exact details of the neuronal circuits involved in ALS have yet to be fully endorsed. To contribute to our understanding of the responsible neuronal circuits, we aimed to investigate the spinal recurrent inhibition (RI) and post-activation depression (P-AD) in ALS patients.
In two groups of ALS patients, i.e. lumbar-affected (clinical signs in leg muscles) and nonlumbar-affected (clinical signs in arms or bulbar region but not in the legs), RI and P-AD on the soleus muscle were investigated using single motor units and amplitude changes of H-reflex in surface electromyography, respectively. The data were compared with healthy subjects.
Compared to controls, P-AD of H-reflex was reduced severely in lumbar-affected patients and reduced to a certain degree in nonlumbar-affected patients. Similarly, a significant reduction in the duration of RI on firing motoneurons was found in lumbar-affected patients (11.5 ± 2.6 ms) but not in nonlumbar-affected patients (29.7 ± 12.4 ms, P < 0.0001) compared to controls (30.8 ± 7.2 ms, P < 0.0001).
The current study revealed that spinal inhibitory circuits are impaired in ALS.
These findings may provide insight for proposing new therapeutic approaches and following disease progression in humans.
Atonic phenomena in focal seizures: Nomenclature, clinical findings and pathophysiological concepts
2012, Seizure
Citation Excerpt :
Transcranial magnetic stimulation studies have shown to not only elicit a positive motor response (motor evoked potential; MEP), but they have shown that such stimulation can also induce a decrease in EMG activity, a phenomenon coined silent period.34–36 This inhibition is caused by spinal mechanisms in the initial phase, whereas cortical inhibitory afferent feedback contributes to the later stages of the silent period.37–40 The generator of this negative motor activity is in close vicinity to the region that produces the positive motor response and most likely overlaps to a large extent with this region.41
Atonic seizures have traditionally been described in patients with generalized epilepsies; however, ictal atonia is increasingly recognized as a phenomenon of focal seizures. Recognition of atonia as a manifestation of focal seizures is crucial in order to not mislabel these events as non-epileptic. In addition, a large number of patients, who undergo presurgical investigations due to focal pharmacoresistant epilepsy, may present with atonia. Therefore, knowledge about the clinical manifestation of atonic seizures and pathological and anatomical insight about the generators of atonia are pivotal to form a hypothesis about the seizure onset zone in epilepsies presenting with such seizures. First, we aim to outline the nomenclature and the definitions in use to describe this enigmatic phenomenon. Second, this paper provides insight into the clinical manifestation and summarizes the cases reported in the literature that meet the criteria of focal atonic seizures. Third, we provide an overview of the current pathophysiological concepts surrounding focal atonia based on the clinical manifestation. This comprehensive review will provide in depth understanding of focal atonic seizures, which will aid in general neurological practice and in the presurgical work up of patients with pharmacoresistant epilepsy manifesting as atonic seizures.
A review of the H-reflex and M-wave in the human triceps surae
2005, Human Movement Science
Citation Excerpt :
Although the antidromically propagating action potential volley elicited by the electrical stimulation in the Ia afferents have no significant effect, the antidromic action potential volley in the motor axons can either collide with the orthodromic sensory (Ia) action potential in the axon or cause hyperpolarisation of the motoneuron soma (Gottlieb & Agarwal, 1976). When collision occurs between the Ia afferent orthodromic volley, and the motor nerve antidromic volley, significant reduction in the H-reflex magnitude will result (Hugon, 1973; Kudina & Pantseva, 1988). This antidromic volley can also collide with voluntarily produced action potentials and therefore reduce the output of the test muscle during the voluntary contraction (Brock, Coombs, & Eccles, 1952).
The soleus is the most commonly used muscle for H-reflex studies in humans, while limited comparable data have been produced from the gastrocnemii muscles. This article reviews the fundamental differences between the structure and function of the human soleus and gastrocnemii muscles, including recent data published about their complex innervation zones. Protocols for eliciting, recording, and assessing the H-reflex and M-wave magnitude in the human triceps surae are also discussed.
Analysis of firing behaviour of human motoneurones within 'subprimary range'
1999, Journal of Physiology Paris
Firing behaviour of human motoneurones within a low range of frequencies was studied during voluntary muscle contraction. It was found that, in contrast to the higher ‘primary range’, both excitability and inhibitibility of these motoneurones were significantly higher. As to their minimal firing rates, no correlation between them and the reciprocal values of afterhyperpolarization (AHP) duration was found. This suggests that AHP can hardly be regarded as the main factor controlling the behaviour of human motoneurones within the low-frequency range of firing and that this range (termed here ‘subprimary range’) should be kept apart from the ‘primary range’.
Recurrent inhibition in humans
1999, Progress in Neurobiology
Methods have been developed to investigate recurrent inhibition (RI) in humans. A conditioning reflex discharge is used to evoke in motoneurones (MNs) supplying homonymous and synergistic muscles, an inhibition the characteristics of which are consistent with RI: it appears and increases with the conditioning motor discharge, has a short latency and a long duration, and is enhanced by an agonist of acetylcholine.
As in the cat, homonymous RI exists in all explored motor nuclei of the limbs except those of the digits and the pattern of distribution of heteronymous RI closely matches that of monosynaptic Ia excitation.
However, striking inter-species differences exist concerning the distribution of heteronymous RI since it is much more widely extended in the human lower limb than in the cat hindlimb, whereas it is more restricted in the upper limb than in the cat forelimb.
Changes in transmission in the recurrent pathway have been investigated during various voluntary or postural contractions involving different (homonymous, synergistic, antagonistic) muscles and it has been found that the activation of Renshaw cells (RCs) by the voluntary motor discharge via recurrent collaterals was powerfully controlled by descending tracts: for example, during homonymous contraction, RI evoked by a given conditioning reflex discharge is much smaller during strong than during weak contraction, which suggests that the descending control of RCs might contribute to the regulation of muscle force.
The finding that RC inhibition is more marked during phasic than during tonic contraction of similar force of the homonymous muscle is discussed in relation with the projections of RCs to Ia interneurones mediating reciprocal inhibition. Only in patients with progressive paraparesis is there evidence for decreased RI at rest which may contribute to the exaggeration of the passively-induced stretch reflex underlying spasticity.
However, despite the seemingly normal RI at rest in most patients, the control of RCs during voluntary movements is disturbed in these patients, which probably contributes to their motor disability.
Independence of motor unit recruitment and rate modulation during precision force control
1999, Neuroscience
The vertebrate motor system chiefly employs motor unit recruitment and rate coding to modulate muscle force output. In this paper, we studied how the recruitment of new motor units altered the firing rate of already-active motor units during precision force production in the first dorsal interosseous muscle. Six healthy adults performed linearly increasing isometric voluntary contractions while motor unit activity and force output were recorded. After motor unit discharges were identified, motor unit firing rates were calculated before and after the instances of new motor unit recruitment. Three procedures were applied to compute motor unit firing rate, including the mean of a fixed number of inter-spike intervals and the constant width weighted Hanning window filter method, as well as a modified boxcar technique. In contrast to previous reports, the analysis of the firing rates of over 200 motor units revealed that reduction of the active firing rates was not a common mechanism used to accommodate the twitch force produced by the recruitment of a new motor unit. Similarly, during de-recruitment there was no tendency for motor unit firing rates to increase immediately following the cessation of activity in other motor units. Considerable consistency in recruitment behavior was observed during repeated contractions. However, firing rates during repeated contractions demonstrated considerably more fluctuation.
It is concluded that the neuromuscular system does not use short-term preferential motor unit disfacilitation to effect precise regulation of muscular force output.

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Main articleRecurrent inhibition of firing motoneurones in man

Abstract

Electroenceph. clin. Neurophysiol.

Brain Res.

The stimulus locked interval histogram: a method that may allow investigation of Renshaw inhibition in man

J. Physiol. (Lond.)

Distribution of recurrent inhibition among motoneurones

J. Physiol. (Lond.)

A comparison of the recurrent inhibition of α- and γ-motoneurones in the cat

J. Physiol. (Lond.)

Relation between shapes of postsynaptic potentials and changes in firing probability of cat motoneurones

J. Physiol. (Lond.)

Changes in recurrent inhibition during voluntary soleus contraction in man studied by an H-reflex technique

J. Physiol. (Lond.)

Main article
Recurrent inhibition of firing motoneurones in man