Reduced excitability of the cortico-spinal system during the warning period of a reaction time task

https://doi.org/10.1016/S0924-980X(98)00050-2Get rights and content

Abstract

Seven subjects made a wrist flexion movement as rapidly as possible in response to a cutaneous shock on the opposite hand. In some trials, an auditory warning signal was given 0.5s beforehand. In random trials, transcranial magnetic stimulation (TMS) was used to elicit EMG responses (MEPs) in forearm flexor and extensor muscles 0–500ms before the cutaneous shock. H-reflexes were elicited in flexor muscles at the same intervals. The warning stimulus reduced reaction time from about 400ms to 200ms. MEPs in the flexor muscles were significantly suppressed from 125ms after the warning stimulus until the time of the cutaneous shock whilst MEPs in the extensors, and H-reflexes in the flexor were either unaffected, or reduced by a smaller amount at a later time. Responses in relaxed contralateral muscles were unchanged. If the task was changed to a choice reaction, in which the imperative stimulus (but not the warning signal) indicated whether to flex or extend the wrist, then there was no change in the MEPs or H-reflex in the warning period. A similar effect was seen if the duration of the warning period was extended from 0.5 to 2s in a simple reaction (flexion) task. We conclude that increased excitability of the corticospinal output is not required to speed up reaction times. The time taken to discharge cortical output elements is relatively unimportant compared with the time needed to process the sensory input and link it to the motor output.

Introduction

Reaction times can be shortened if a warning signal is given prior to the imperative stimulus. It is thought that the presence of the warning signal reduces the temporal uncertainty of the imperative signal. Thus, the longer and more variable the interval between warning and imperative signal, the smaller the effect on reaction time (Bock and Lincoln, 1988). Maximum shortening of reaction time occurs when the warning signal precedes the imperative signal by a regular interval of about 0.2–0.5 s. The heightened responsiveness of the reaction system may be due either to shortening of the processing time for identification of the imperative signal, or to increased preparation of the motor response, or to both. In either case, the nervous system has the task of maintaining heightened excitability whilst at the same time preventing escape of the response until the imperative signal is identified correctly.

The aim of the present experiments was to test whether increased excitability of the corticospinal outflow during the warning period contributes to the decrease in reaction time. Previous experiments (Evarts and Tanji, 1976; Tanji and Evarts, 1976) on monkeys suggest very strongly that this should be the case. During the interval between an instructional warning stimulus and a reaction signal, 61% of precentral pyramidal tract neurones changed their discharge according to the nature of the instruction. For example, neurones that usually discharged during the push movement also increased their firing rate if the warning signal indicated that a push movement was about to occur whereas neurones that discharged in relation to the pull movement would decrease their firing. The implication of these results is that the excitability of the motor cortical projection to agonist muscles may be increased during a warning period.

Work on spinal reflexes has extended these concepts. Brunia and colleagues (Brunia and Vuister, 1979; Brunia et al., 1982) examined spinal reflexes during a 4 s warning period, and proposed that three types of reflex changes occur. Immediately after the warning signal, reflexes in both involved and non-involved muscles increase perhaps reflecting arousal produced by the stimulus. Thereafter, the responses in the future agonist may decrease slightly, whereas those in other muscles continue to increase. After the imperative signal has been received there is a clear increase in agonist excitability over and above that seen in other muscles. The persistent increase in spinal reflexes in the warning period was thought to be due to facilitatory corticospinal influences. The late suppression of agonist reflexes in the latter part of the warning period was postulated to be due to presynaptic inhibition of Ia afferents.

There is little information in humans about the effect of a warning signal on excitability of cortical mechanisms. Most studies using transcranial magnetic stimulation (TMS) have not used a warning stimulus and have therefore been limited to the period between the imperative signal and the onset of the voluntary response (Pascual et al., 1992). In one recent study, TMS was delivered in the period between the warning signal and the imperative signal in a reaction time task (Hasbroucq et al., 1997). Responses, which were measured only in the agonist muscle, were decreased during the latter part of the warning period. This suggests a decrease in cortico-spinal excitability during preparation for movement but does not indicate if this change is specific or generalized, or whether it reflects an effect at a cortical or spinal level. Using a different approach, Bonnet (1983)showed that the M2 component of the stretch reflex in wrist muscles increased during a 2 s warning period, and interpreted this as evidence for increased cortical excitability. However, recent work has cast doubt on whether the M2 response in these muscles is a transcortical response as they had assumed (Meyer et al., 1992). It seems more likely that it is a long latency spinal response mediated by slow conducting group II afferents.

The present experiments used TMS to test corticospinal excitability directly during a warning period. We measured responses in agonist, antagonist and contralateral muscles and used H-reflexes to examine reflex excitability changes. We used a short (0.5 s) warning period in order to produce a clear reduction in reaction time, so that any preparatory processes would be functioning at maximum effectiveness. We found that the cortico-spinal excitability as tested by transcranial magnetic stimulation was decreased during the warning period, particularly the projections to the future agonist muscle. Part of this work has been published previously in abstract form (Touge et al., 1993).

Section snippets

Methods

Subjects were 15 normal volunteers (12 male and 3 female, age range 28–44 years) and were studied with informed consent and the approval of the local ethical committee. They sat in comfortable chair with their arm well supported. Every 8 s or so, an auditory warning signal was given (1 kHz, 50 ms duration) via an earphone, and this was followed 0.5 s later by a small cutaneous stimulus (200 μs duration 4 times perceptual threshold) given through electrodes over the back of the left hand. The

Reaction time effect

The reaction time to the imperative signal in conditions 1, 2, 4 and 5 of the simple wrist flexion task is shown in Fig. 2. The reaction time to the imperative stimulus alone was rather long, but this was probably because it was interspersed between a majority of trials in which warnings were given. As expected, the presence of the warning signal speeded up reaction time (compare condition 1 and 4: P<0.05). Interspersing magnetic test stimuli between warning and imperative signals had no effect

Discussion

In the present experiments, a warning signal was given 0.5 s before an imperative stimulus. This reduced the reaction time of a simple wrist flexion/extension task by almost half, from about 400–200 ms. Unexpectedly, magnetic stimulation suggested that during the warning period, the excitability of the corticospinal system to the future agonist muscle decreased rather than increased.

There have been several previous studies in which corticospinal excitability has been examined after the

Acknowledgements

We should like to thank Mr. R. Bedlington for maintaining and constructing much of the equipment used in these experiments.

References (16)

There are more references available in the full text version of this article.

Cited by (81)

  • TMS reveals distinct patterns of proactive and reactive inhibition in motor system activity

    2022, Neuropsychologia
    Citation 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).

View all citing articles on Scopus
View full text