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REPORT
Laboratoire de Plasticité et PhysioPathologie de la Motricité, Unité Mixte Recherche 6196, Centre National de la Recherche Scientifique/Université de la Méditerranée, Marseille Cedex 20, France
Submitted 22 September 2004; accepted in final form 13 November 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Jankowska 1992). It has been established that the excitability of these inhibitory pathways depends on the subject’s posture (Kasai et al. 1998; Kido et al. 2004) and on whether agonist or antagonist muscles are contracted (Aimonetti et al. 2001; Cavallari et al. 1984; Kato and Kasai 2000). Even in the absence of any actual contractions, mental simulation of motor actions can affect the inhibitory effects of antagonist Ia afferents (Nielsen et al. 1995). In a previous study (Nafati et al. 2004), we observed that the homonymous Ia monosynaptic proprioceptive feedback acting on wrist extensor motoneurons was enhanced during an attention-demanding visuomotor task. The aim of the present study was therefore to examine the inhibitory control exerted by the antagonist Ia afferents from wrist flexor muscles under the same conditions. The hypothesis was put forward that this inhibitory control may increase during the performance of an attention-demanding task and thus maintain the balance between the excitatory and inhibitory inputs acting on the wrist extensor motoneurons. |
METHODS |
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Procedure
Details of the experimental set-up, preparation of the subjects, data recordings, and the equipment used have been described previously (Nafati et al. 2004; Schmied et al. 2000). The subjects were seated in an adjustable armchair. Their right forearm was placed in a groove, and the distal end was immobilized. The hand was placed in a semi-prone position, with the wrist flexed at an angle of 10°, while the back of the hand was in permanent contact with an isometric force transducer device (DC gain, 0.25 V/N). The subjects had to selectively contract their wrist extensor muscles by pushing on the force transducer device with the back of their hand. The force was monitored on an oscilloscope screen (sweep rate: 0.5 ms/division), and the subjects were required to maintain the level of extension force as steady as possible by tracking a horizontal line located in the middle of the oscilloscope screen. Two gains in the force feedback were used alternately in two successive randomized recording sequences. The two gains differed by a factor of 50: a change of 0.1 N in the force output gave an oscilloscope trace deviation of 0.05 divisions at low gain and 2.5 divisions at high gain. The activity of single motor units (SMUs) was recorded in the extensor carpi radialis muscle (ECR) using tungsten microelectrodes. The subjects were asked to contract the ECR muscle and to maintain an extension force above the recruitment threshold (RT) of the motor unit under investigation so that its tonic firing rate was 
10 Hz. In these experiments, the level of the extension force was <10% of the maximum voluntary contraction and only low-threshold SMUs were tested (RT < 1 N). The electromyographic activity of the extensor and flexor muscles was recorded using pairs of surface electrodes (surface EMG).
Stimulation paradigm
The effects of the median nerve electrical stimulation on the voluntary tonic discharge of extensor single motor units were investigated under the two feedback conditions in two successive recording sequences. Responses to 40–60 stimuli were collected throughout each sequence lasting 2–3 min. Resting periods of 1–2 min were allowed to elapse between the sequences. Before each series of experiments, the median nerve stimulation was progressively increased in such way as to evoke a clear-cut H-wave (Hoffmann reflex, H-reflex) in the flexor carpis radialis muscle (FCR), which reflected the effectiveness of the group Ia afferent activation, just below the M-wave threshold. The FCR H-reflex was elicited by applying cathodic stimulation to the median nerve in the cubital fossea and the anode was placed opposite the cathode. The stimulus intensity was set at 0.8 the motor threshold. The cathodic stimulation (pulse duration: 0.5 ms) was delivered using a spike-triggered stimulation method (Jones and Bawa 1995; Nafati et al. 2004). The spikes produced by voluntarily activated motor units were discriminated on-line and the output TTL pulses were used to trigger the stimulator (Grass S88, USA) after a fixed delay with respect to the motor unit potential. In this study, a spike-to-stimulus delay of 40 ms was used. Stimuli were delivered with a minimum time interval of 3 s.
Data analysis
The inhibitory effects of the median nerve stimulation on the tonic activity of ECR motor units were analyzed in terms of the interspike interval (ISI) lengthening. The spike trains were displayed in the form of trial-by-trial rasters, and peristimulus time histograms (PSTH) of the motor unit discharge were drawn up using Spike 2 software (CED Cambridge, UK). The durations of the ISIs around each stimulation were computed, including the ISI during which the stimulus occurred (stimulus ISI, ISI 0), the following ISI (poststimulus ISI, ISI +1), and the prestimulus ISI (ISI –1), which was obtained by averaging the three preceding ISIs (Fig. 1). The value of ISI –1 was taken as an estimate of the motor unit’s instantaneous background activity. The mean durations of ISI –1, ISI 0, ISI +1 were calculated for each SMU.
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The mean ISI –1, mean ISI 0, mean ISI +1, the mean forces, and the mean EMGs were compared between the two conditions, using a paired sample Wilcoxon test. The condition-related changes in the ISI durations were assessed in each single motor unit by performing a Mann and Whitney test on the absolute values. The significance level was set at P < 0.05.
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RESULTS |
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The visual force feedback-related changes in the ISI duration were assessed by examining the tonic firing activity of 31 wrist extensor motor units. Figure 2 shows a typical example of the changes observed in a single motor unit. In this example, no differences were detected between the prestimulus ISI (ISI –1) tested under low- and high-gain force feedback conditions (86.9 ± 7.2 and 86.1 ± 7.6 ms, respectively). The stimulus ISI (ISI 0) was significantly longer than the prestimulus ISI (ISI –1) in both conditions (90.8 ± 4.9 and 99.3 ± 5.4 ms, low and high gain, respectively; P < 0.05), in keeping with the inhibitory effects of the median nerve stimulation in both situations. The main result illustrated by this example was that the lengthening of the stimulus ISI (ISI 0) was significantly greater under high-gain than low-gain conditions (P < 0.05). The median nerve stimulation did not affect the duration of the poststimulus ISI (ISI +1) in either of the conditions (85.5 ± 9.1 and 84.2 ± 10.8 ms, low and high gain, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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When the activity of single motor units was being recorded in humans, the effects of stimulating the antagonist Ia group afferents were previously assessed in terms of the firing probability in poststimulus time histograms, which showed a decrease (Aimonetti et al. 2000, 2001; Ashby and Label 1977; Nielsen and Kagamihara 1992). In the present study, the effects of median nerve stimulation on the tonic firing pattern of voluntarily activated wrist extensor motor units were analyzed in terms of the interspike interval duration. Analyses of this kind are particularly helpful means of assessing the inhibitory effects of a stimulation-elicited afferent volley on the spike trains of individual motor units (Garland and Miles 1997). Here we observed a lengthening of the ISI in which the Ia afferent volley occurred, in keeping with the expected inhibitory effects of the antagonist primary afferent stimulation.
The stimulation was elicited 40 ms after the triggering spike. The earliest inhibitory processes induced by the antagonist Ia afferent volleys can therefore be expected to reach the motoneuron 60 ms after the triggering spike was generated (40 ms + mean FCR H-reflex latency). Consequently, the inhibitory processes observed in the present study should last from 20 to 40 ms at least to be able to affect the next spike, which can be expected to occur 80–100 ms after the triggering one in the absence of stimulation (minimum ISI –1: 77.6 ms and maximum ISI –1: 96.1 ms).
Besides the disynaptic reciprocal inhibition lasting <10 ms (Aimonetti et al. 2001; Crone 1993), later and/or longer lasting synaptic effects are liable to contribute to the inhibitory responses observed. This contribution includes the late inhibitory response (latency : 30–40 ms) that follows the disynaptic one (Aimonetti et al. 2001; Crone 1993). It is therefore quite likely that under the present experimental conditions, part of the ISI 0 lengthening induced by median nerve stimulation may have involved polysynaptic pathways in addition to the disynaptic one. On the other hand, the possible contribution of the recurrent inhibition pathway cannot be excluded, given its specific pattern of organization in the motor nuclei of the wrist extensor and flexor muscles (Aymard et al. 1997). However, the strength of this possible recurrent interaction would probably be weaker than that of the reciprocal inhibition (Windhorst 1996).
Possible mechanisms involved in changes in antagonist inhibition
The present results show that the efficiency of the inhibitory pathways fed by the antagonist Ia muscle afferent is enhanced when the wrist extensor motoneurons are involved in an attention-demanding task. These changes in inhibitory strength cannot be due to changes in the level of extensor motoneuron excitability as no significant differences were detected between the mean prestimulus ISIs analyzed under low- and high-gain conditions, and the effects of the antagonist afferent sensory burst were tested at a specific time during the interspike interval. In addition, in a previous study using the same experimental procedure, we obtained convincing findings showing the consistency of the motor output between the two visual force feedback conditions (Nafati et al. 2004).
The fact that the ISI during which the stimulation was delivered showed a greater lengthening under high-gain conditions may reflect an increase and/or a lengthening of the composite IPSPs generated by the median nerve stimulation. These changes may have resulted from the action of descending inputs on the Ia inhibitory interneurons from flexor to extensor muscles (Crone and Nielsen 1994; Jankowska et al. 1976; Nielsen et al. 1992), which would facilitate transmission in the reciprocal inhibitory pathways when special attention was required by the motor task This central modulation of the group Ia inhibitory interneurons may be exerted via propriospinal neuron relays (Alstermark et al. 1984; Pierrot-Deseilligny 1989). Enhanced excitability in the neural pathways mediating antagonist inhibition might also result from an increase in the Ia afferent inputs to premotoneuronal inhibitory interneurons, resulting either from an attention-related decrease in presynatic inhibition of flexor Ia afferent terminals on Ia inhibitory interneurons (Enriquez-Denton et al. 2000) and/or from an increased on-going spindle discharge rate. The latter assumption is in keeping with the data obtained in our former study, suggesting that a fusimotor-drive activation occurs under high-gain visual force feedback conditions (Nafati et al. 2004). This activation would therefore be likely to increase the resting discharge of the flexor muscle spindles (cf. Rossi-Durand 2002). This may result in either the facilitation of premotoneuronal inhibitory interneurons, making them more responsive to the median nerve stimulation, or the activation of alternative polysynaptic pathways, such as propriospinal pathways, that were inactive under low gain conditions (cf. Crone 1993).
Functional implications
The increase in the reciprocal inhibitory control exerted by the antagonist flexor afferents during attention-demanding tasks would compensate for the increase in the autogenic excitatory control exerted by the homonymous muscle spindle afferents that we previously observed under the same conditions and would thus contribute to maintaining the balance between excitatory and inhibitory inputs to the wrist extensor motoneurons.
This modulation of the antagonist proprioceptive inhibitory control depending on the level of attentiveness required by the task may be one of the processes involved in the fine adjustment of the wrist muscle force output required in accurate handling tasks.
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: C. Rossi-Durand, Laboratoire de Plasticité et PhysioPathologie de la Motricité (P3M), UMR 6196, CNRS/Université de la Méditerranée, 31, chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France (E-mail: crd{at}dpm.cnrs-mrs.fr)
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REFERENCES |
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Aimonetti J, Vedel J, Schmied A, and Pagni S. Changes in the tonic activity of wrist extensor motor units induced by stimulating antagonistic group I afferents in humans. Exp Brain Res 141: 21–32, 2001.[CrossRef][Web of Science][Medline]
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Cavallari P, Fournier E, Katz R, Pierrot-Deseilligny E, and Shindo M. Changes in reciprocal Ia inhibition from wrist extensors to wrist flexors during voluntary movement in man. Exp Brain Res 56: 574–576, 1984.[Web of Science][Medline]
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Enríquez-Denton M, Nielsen J, Perreault MC, Morita H, Petersen N, and Hultborn H. Presynaptic control of transmission along the pathway mediating disynaptic reciprocal inhibition in the cat. J Physiol 526: 623–637, 2000.
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, the ISI in which the stimulation occurred (ISI 0). Top: a schematic representation of the interspike intervals (ISIs) analyzed. The value of the prestimulus ISI (ISI –1) was obtained by averaging the 3 preceding ISIs. The durations of ISI –1, ISI 0, and ISI +1 in response to each stimulus applied to the median nerve were calculated.
