Research reportPreparatory inhibition of cortico-spinal excitability: a transcranial magnetic stimulation study in man
Introduction
Motor preparation has been extensively investigated through the study of the effect of foreperiod duration on reaction time [1]. These studies have shown that preparation is a short lasting, fatigue-sensitive process. Because preparation can be optimal only for a few milliseconds, it is set according to the subject's expectations concerning the occurrence of the reponse signal. For instance, when the duration of the foreperiod (i.e., the interval between a warning signal and the response signal) is varied across blocks of trials, the subject times his (her) preparation so he (she) can be optimally ready at the onset of the response signal. However, reaction time (RT) lengthens as the duration of the foreperiod is increased [34], because the accuracy of this timing decreases as the time elapsed since the warning signal lengthens 13, 25. Studies combining reflex techniques with simple RT protocols have revealed a neural correlate of motor preparation. They have shown that the subjective state of readiness induces systematic variations in the excitability of the spinal motor structures (for reviews see refs. 4, 25). When the duration of the foreperiod is constant within a block of trials, the amplitude of monosynaptic reflexes (Hoffmann (H) and Tendinous (T)), triggered in a prime mover, decreases prior to the onset of the response signal. This decrement which was first observed with a foreperiod of 1 s (for reviews, see refs. [6]and [26]) has been confirmed with foreperiods of longer duration 5, 6, 7, 8, 29. However, with long foreperiods, the decrement in the amplitude of reflexes triggered in the involved muscle is essentially relative to the amplitude of reflexes elicited in a non-involved muscle. This reflex depression is thought to reflect the presynaptic inhibition of the motoneurons' somesthetic afferents, which increases the sensitivity of the motoneuronal pool to supraspinal commands 26, 30.
However, whilst most results concerning the effects of preparation on RT have been obtained in manual key-pressing tasks, the conclusions concerning the preparatory modulations of spinal excitability have been exclusively reached from the study of reflexes elicited in a lower limb muscle, the soleus. This is probably because, in the manual RT tasks traditionally designed to study the effects of preparation, the prime movers are at rest during the foreperiod. This condition precludes reflex investigations in the upper limb muscles where monosynaptic responses can be obtained only during voluntary contraction (see ref. [9]). In contrast, H or T stimulations easily elicit reflex responses in the soleus, even when this muscle is at rest (e.g. ref. [20]). As stressed by Bonnet et al. [4], the reflex sensitivity of the soleus is related to its functional features. In particular, the soleus is mainly used in postural activities involving the antigravity servo-control of neuromuscular spindles. To subserve this function, it comprises a high proportion of small tonic motor units which are more sensitive to proprioceptive Ia afferents than the motor units composing the upper limb muscles. In humans, the upper limb muscles have a quite different function: they are mainly involved in phasic non-postural activities, such as reaching or key-boarding. Because of this functional difference, generalization to upper limb muscles of conclusions drawn from the study of reflexes elicited in the soleus appears unwarranted. Indeed, little is known concerning the preparatory modulations of the excitability of the neural structures controlling the muscular activity of the upper limbs. In order to decipher these processes, research can be pursued in two complementary directions. First, preparatory reflex modulations in upper limb muscles could be studied during tonic voluntary contractions. The second direction is to study the modulations of the motor potentials evoked in the upper limb muscles at rest by the transcranial magnetic stimulation (TMS) of the motor cortex. The present study has been performed in the latter perspective.
Transcranial magnetic stimulation of the motor cortex produces contralateral motor evoked potentials (MEPs) in upper limb muscles at rest. It is generally considered that inframaximal TMS induces electrical currents which excite cortical interneurons projecting onto the cortico-fugal cells of the pyramidal tract. The variability of the MEPs seems to be one of their characteristic features: even when elicited with identical stimuli, their within-subject amplitudes vary from trial to trial 2, 10, 16, 19. The premice of the present study was that the level of preparation attained by the subjects could be a systematic source of variance in the amplitude of the MEP amplitude evoked in a prime mover by the TMS of the motor cortex. In the context of the study of preparation, the main interest of the TMS is that it can be delivered during the performance of tasks similar to those classically designed to study the effect of preparation on information processing. The behavioral protocol used in the present experiments originates in a recent study of Hasbroucq et al. [15]where the activity of the flexor digitorum sublimis was investigated. In the present study, the coil was oriented so as to induce a postero-anterior electric field in the area of the motor cortex controlling this muscle. A drawback of this procedure is that it does not allow one to dissociate the modulations of motoneuronal excitability from those of cortical cells1.
In the first experiment, two foreperiod durations were used, namely 500 ms and 2500 ms. According to Bertelson [3], 500 ms could be about the optimal delay for attaining a maximal level of preparation. In agreement with this, Hasbroucq et al. [15]have recently shown that the subjects attain a much higher level of preparation for a foreperiod of 500 ms than for a foreperiod of 2500 ms. Therefore, these two values were used in the present study in an attempt to manipulate the state of readiness of the subjects. In experiment 1, the TMS was delivered either simultaneously with the warning signal or simultaneously with the response signal. The results of this experiment show that, for the long foreperiod, the time of stimulation has no detectable effect whereas, for the short foreperiod, the amplitude of the MEP decreases as the time elapses. Experiment 2 was performed in an attempt to refine this analysis by tracking the time-course of the cortico-spinal excitability during the 500 ms foreperiod. With this aim, the TMS was delivered either 500, 333, 167 or 0 ms before the response signal whilst the subjects were performing the short foreperiod condition of experiment 1. The decrement of cortico-spinal excitability was effective during the first 333 ms and then remained stable until the occurrence of the response signal.
Section snippets
Subjects
After being informed of the purpose and techniques of the study, 14 healthy members (1 woman and 13 men) of the National Institute of Bioscience and Human Technology (Tsukuba, Japan) volunteered for the experiments. They were aged between 28 and 40 years (mean=32). All of them were right-handers and had normal or corrected-to-normal visual acuity. Ten subjects were run in each experiment. Six subjects participated in the two experiments. Experiment 2 was performed 20 months after experiment 1.
Transcranial magnetic stimulation
A
Error rate
For the no-stimulation trials, the error rate was 2.92%. The arcsine transforms of the frequency of errors per subject and condition of foreperiod duration (short, long) and response effector (index, middle finger) were submitted to an ANOVA that used the mean square of the interaction between the effect of the subject and the effect of the factor under analysis as the error term. This ANOVA involved foreperiod duration and response effector as within-subject factors. None of these two factors
Discussion
The present study was performed in an attempt to explore the preparatory modulations of cortico-spinal excitability by combining the methods of mental chronometry (cf. [21]) with the technique of TMS. Motor potentials were evoked in the flexor digitorum sublimis at rest by stimulation of the motor cortex during the foreperiod of a manual choice RT task. Experiment 1 evidenced a decrease in cortico-spinal excitability during a short foreperiod (500 ms) but not during a long foreperiod (2500 ms).
Acknowledgements
This work was supported by a grant of the Direction de la Recherche et des Etudes Techniques under Contract 93/095. We thank Michel Bonnet and Isabelle Mouret for many fruitful discussions. We are indebted to Allen Osman and to two anonymous reviewers for their helpful comments on a preliminary version of this article.
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2022, NeuropsychologiaCitation Excerpt :However, the trend indicates that it is not cue B that is “released from inhibition” but that corticospinal excitability reduces for cue A. One possible explanation for the reduction in activity to cue A is that participants are engaging in a form of impulse control (e.g., Hasbroucq et al., 1997; Touge et al., 1998; Davranche et al., 2007; Duque and Ivry, 2009) to prevent premature responding to a highly probable X probe. An alternative explanation is that the motor system reduces excitability following an A cue, rather than sustaining it, to conserve metabolic energy when a response is not yet required (see Tran et al., 2021a or Tran and Livesey, 2021 for another possible explanation that is beyond the scope of this discussion on motor control).