Elsevier

Cognitive Brain Research

Volume 24, Issue 3, August 2005, Pages 355-363
Cognitive Brain Research

Research Report
Listening to action-related sentences modulates the activity of the motor system: A combined TMS and behavioral study

https://doi.org/10.1016/j.cogbrainres.2005.02.020Get rights and content

Abstract

Transcranial magnetic stimulation (TMS) and a behavioral paradigm were used to assess whether listening to action-related sentences modulates the activity of the motor system. By means of single-pulse TMS, either the hand or the foot/leg motor area in the left hemisphere was stimulated in distinct experimental sessions, while participants were listening to sentences expressing hand and foot actions. Listening to abstract content sentences served as a control. Motor evoked potentials (MEPs) were recorded from hand and foot muscles. Results showed that MEPs recorded from hand muscles were specifically modulated by listening to hand-action-related sentences, as were MEPs recorded from foot muscles by listening to foot-action-related sentences. This modulation consisted of an amplitude decrease of the recorded MEPs. In the behavioral task, participants had to respond with the hand or the foot while listening to actions expressing hand and foot actions, as compared to abstract sentences. Coherently with the results obtained with TMS, when the response was given with the hand, reaction times were slower during listening to hand-action-related sentences, while when the response was given with the foot, reaction times were slower during listening to foot-action-related sentences. The present data show that processing verbally presented actions activates different sectors of the motor system, depending on the effector used in the listened-to action.

Introduction

We can understand actions done by others both when we observe these actions while being done and when we hear about them verbally. There is increasing evidence that there is a neural system formed by a particular set of premotor neurons, called “mirror neurons”, that plays a role in action understanding [6], [23], [41], [45].

Mirror neurons were originally discovered in the monkey ventral premotor cortex (area F5). Their characterizing property is that they discharge both when the monkey performs specific goal-directed hand or mouth actions (i.e., grasping, tearing, holding, biting, sucking) and when it observes another individual performing the same or a similar action [17], [21], [43]. Mirror neurons were also described in the inferior parietal lobule [22], thus constituting a parieto-premotor circuit (mirror neuron system) for action understanding. Recently, it has been shown that many F5 mirror neurons, besides having visual properties, also have acoustic properties. These “audio-visual mirror neurons” discharge not only when the action is executed or observed, but also when its sound is heard [32].

A mirror neuron system similar to that described in the monkey has been also found in humans. Experimental evidence in this sense comes from neurophysiological, behavioral, and brain imaging studies. Using single-pulse transcranial magnetic stimulation (TMS), it was demonstrated that, during the observation of hand and arm movements, there is an increase of motor evoked potentials (MEPs) recorded from hand muscles involved in the actual execution of the observed movements [14], [46]. A recent TMS study further showed that, during the observation of hand actions, there is a temporal modulation of the MEPs recorded from the hand muscles of the observer, which follows the temporal progress of the observed action [24]. Taken together, these results strongly suggest that the mirror neuron system matches the observed action with its motor representation in the observer, both in terms of the muscles involved and the temporal progress of the action.

The involvement of the mirror neuron system during action observation was also demonstrated using magnetoencephalography (MEG). With this technique, a suppression of the 15- to 25-Hz activity during both the execution and observation of goal-directed hand actions was found [29]. Similar results were obtained in a quantified electroencephalography study, showing a block of “mu” activity in the same conditions [9]. More recently, it was shown by means of chronically implanted subdural electrodes, a decrease of alpha band absolute power over the primary motor cortex and Broca's region during the execution and observation of finger movements [50].

Behavioral studies also demonstrated that action observation may modulate the activity of the motor system [4], [11], [51]. Brass et al. [4], using a reaction time (RTs) paradigm, compared the efficiency of symbolic cues with direct observation of finger movements done by another person in triggering finger movements. The results showed that participants were faster in lifting their fingers when the relevant cue for their response was the observation of the same finger movement, as compared to the symbolic cue. Similar results were obtained by Craighero et al. [11] in a study in which participants were required to prepare to grasp a differently oriented bar, after presentation of a picture showing the right hand. Participants were faster when the orientation of the observed hand corresponded to that achieved by the participants' hand at the end of the action.

These studies do not provide, of course, information on the localization of the mirror neuron system. Brain imaging experiments addressed this issue. These studies showed that during the observation of hand/arm actions, there was signal increase in the ventral premotor cortex and the adjacent posterior part of the inferior frontal gyrus (IFG), and in the inferior parietal lobule [13], [26], [27], [28], [44]. Thus, similarly to monkeys, in humans, the mirror neuron system also appears to be localized in the ventral premotor cortex and in the inferior parietal lobule. Furthermore, in a functional magnetic resonance (fMRI) study, it was shown that during the observation of hand, mouth, and foot actions, there is a selective activation of different sectors of the premotor cortex, the adjacent IFG, and of the inferior parietal lobule, depending on the effector involved in the observed action [5]. These results not only extend the domain of the mirror neuron system to effectors other than the hand, like the mouth and the foot, but also show that this system is somatotopically organized.

As mentioned above, the main functional role of the mirror neuron system appears to be that of understanding actions done by others. This appears to be true also when the observed action is done by non-conspecifics (monkey, dog), provided that the observed action belongs to the motor repertoire of the observer [7]. In humans, the mirror neuron system appears to be also involved in the imitation of hand and mouth actions present in the observer's motor repertoire [31], [34], [35], [48]. Recent evidence showed that the mirror neuron system is also involved in imitation learning of novel complex actions [8].

Given the homology between the monkey's premotor area F5 and Broca's region [37], [52], it has been suggested that the mirror neuron system represents the neural substrate from which human language evolved [1], [10], [40], [42]. It is an open question, however, whether, in modern humans, this system plays a role in understanding the meaning of sentences.

The meaning of a sentence, regardless of its content, is classically considered to be understood by relying on symbolic, amodal mental representations [18], [39]. An alternative hypothesis assumes that the understanding of language relies on “embodiment” [3], [16], [20], [25], [33], [38]. Thus, for action-related sentences, the neural structures presiding over action execution should also play a role in understanding the semantic content of the actions verbally described.

A prediction of the embodiment theory of language understanding is that when individuals listen to action-related sentences, their mirror neuron system is modulated. The aim of the present study was to test this hypothesis. Two experiments were carried out: in Experiment 1, we recorded, in two distinct sessions, motor evoked potentials (MEPs) from hand and foot muscles, respectively, while participants were listening to hand-action-related sentences, foot-action-related sentences, and abstract content sentences; in Experiment 2, a similar task was used in a go/no-go paradigm. The results clearly show the involvement of the motor system in the processing of action-related sentences.

Section snippets

Experiment 1: TMS study

The aim of this study was to assess whether listening to action-related sentences modulates the activity of the primary motor cortex, as revealed by MEPs recorded from hand muscles when stimulating the hand motor area, and from foot/leg muscles when stimulating the foot motor area. In order to verify not only a possible modulation of MEPs, but also its specificity, related to the effector involved in the listened action, we presented sentences describing hand and foot actions. Abstract content

TMS study

The ANOVA carried out on MEPs recorded from first dorsal interosseus and opponens pollicis after single-pulse TMS of the hand motor region showed that only the main effect of “sentence” was significant, F(2,14) = 5.85, P < 0.02, demonstrating that MEP amplitude decreased specifically during listening to hand-action-related sentences with respect to the other two types of sentences. The Mauchley's test showed that the sphericity assumption was not violated (P > 0.05). No significant difference

Discussion

The main finding of the present study was a clear modulation of the activity of the motor system during listening to sentences expressing foot/leg and hand/arm actions. This modulation was specific for the effector involved in the listened-to action. Listening to hand-action-related sentences induced a decrease of MEP amplitude recorded from hand muscles. Similarly, listening to foot-action-related sentences induced a decrease of MEP amplitude recorded from foot muscles. Listening to abstract

Acknowledgments

This work was supported by the European Science Foundation EUROCORES program “The Origin of Man, Language and Languages”, by the European grant Mirrorbot Contract n. IST 2001-35282, by VolkswagenStiftung, and by MIUR (Ministero Italiano dell'Istruzione, dell'Università e della Ricerca).

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