Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study
Introduction
Electrophysiological evidence recently showed that actions are stored in the brain as goal related motor schemes. Single unit recordings performed in the monkey ventral premotor cortex (area F5) demonstrated that neurons in this region selectively discharge during goal-directed hand actions [37]. The specificity of the goal seems to be an essential prerequisite in activating these neurons: the same neurons that discharge during grasping, holding, tearing, manipulating, are silent when the monkey performs actions that involve a similar muscular pattern but with a different goal (i.e. grasping to put away, scratching, grooming, etc.). Many grasping neurons, the most represented class of hand related F5 neurons, are selective for a particular type of prehension (precision grip, finger prehension, whole hand prehension) [37]. All these data indicate that in the ventral premotor cortex a vocabulary of actions is stored 37, 38. The presence of such a vocabulary may strongly facilitate the execution of motor commands and endows the brain with a storage of action schemes related to the specification of action goals [23]. Thisvocabulary of actions can be addressed not only during action execution. Recent experiments have shown that many F5 neurons (canonical neurons) discharge at the mere visual presentation of objects whose shape and size is congruent with the type of grip coded by the same neurons 31, 37. A second class of F5 grasping neurons, mirror neurons, are selectively activated when the monkey observes another individual performing actions similar to those they motorically code [18]. It was proposed that mirror neurons represent an observation/execution matching system, possibly involved in understanding actions made by others. The properties of both canonical and mirror neurons demonstrate that the same pool of motor schemes can be visually addressed either by objects or by action observation. The possibility to visually address a similar motor vocabulary in humans was demonstrated by a recent experiment in which the excitability of the corticospinal system was tested by transcranial magnetic stimulation (TMS) while subjects observed a series of goal-related hand actions performed by the experimenter in front of them [16]. During action observation, the motor evoked potentials (MEPs) recorded from subjects hand muscles significantly increased with respect to different control conditions. In addition, the observed pattern of hand muscle facilitation was congruent with that observed during actual execution of similar actions. The activation of action vocabulary either during the execution of transitive movements or during observation of objects or of actions performed by others, is triggered by the presence of external stimuli. On the other hand, the evolutionary process has provided the human brain with the possibility to mentally represent things (actions, objects, emotions, etc.) by means of the voluntary process of thought, also in the absence of any external trigger. It is a common experience that we can mentally represent actions simply by thinking about them. This process of mental representation of movements is usually defined as motor imagery. According to Jeannerod [22]: Motor imagery would be a part of a broader phenomenon (the motor representation). During motor imagery, the subject looks at its own motor repertoire and feels himself to move from the inside. The idea that motor imagery could share phenomenological aspects with movement execution is supported by several findings: (1) The main vegetative parameters, such as heart rate, blood pressure, and breath frequency significantly increase during mental simulation of movements strictly correlating with the strength of the effort[11](2) The duration of imagined actions is similar to that of the same actions when actually executed [12]; (3) Many brain imaging studies showed an increase of regional cerebral blood flow (rCBF) in various cortical motor areas and cerebellum during motor imagery tasks 13, 17, 19, 36, 39, 41, 44, 47. Similar results were recently achieved by magnetoencephalography 20, 45and movement related potentials 5, 9. It is not completely clear, however, if these movement-related phenomena are due to unspecific factors such as intention or readiness to move, or if they rather reflect a true internal dynamic simulation of movement. This issue can be addressed by using TMS, a technique that allows one to measure the corticospinal excitability with high sensitivity and, most importantly, with high temporal resolution, thus providing a precise description of the excitation/inhibition pattern present in the corticospinal system at the moment of the stimulation 4, 28, 42.The reliability of this technique in revealing the gross modulation of corticospinal excitability exerted by movement simulation, cortical plasticity and motor learning was previously shown by several authors 1, 24, 33, 34, 35, 48, 49. In the present paper we will present the results of two TMS experiments in which we investigated the problem of the specificity of action representation and dynamics during motor imagery. In the first experiment the excitability of arm and hand muscles was assessed by stimulating the left precentral cortex during mental simulation of right forearm extension and flexion and right hand opening and closing. In the second experiment, in addition to the specific effect induced by imagined movements on hand muscles, the different contribution of the two hemispheres to motor imagery of ipsilateral and contralateral hand movements was also investigated.
Section snippets
Subjects
Six, right handed, human subjects (2 males and 4 females) participated in the experiment. Age ranged from 23 to 35 (mean, 28). All of them, but one (author), were naive as to the purpose of the experiment and gave their informed consent. The experimental procedure was approved by the Parma University Ethical Committee.
2.2.1. Session 1 (proximal arm motor imagery)
Fig. 1 shows the individual data recorded from one subject (upper four panels) and mean z-score of BB MEP areas recorded during imagined forearm extension and flexion expressed as difference from the control condition (visual imagery of expanding-shrinking bar). Statistical analysis showed that the two imagined movements differently affected the excitability of BB muscle (t-student test: t(5) = −3.2, P < 0.05): MEP amplitude was larger during motor imagery of forearm flexion than during motor
3.1.1. Subjects
Six, right handed, human subjects (4 males and 2 females), different from those of Experiment 1, participated in the experiment. Age ranged from 24 to 31 (mean, 26). All subjects were naive as to the purpose of the experiment and gave their informed consent to the experimental procedure that was approved by the University of Parma Ethical Committee.
3.1.2. Procedure
The general experimental set up was the same as in Experiment 1. Intwo different experimental sessions, left and right motor cortex were stimulated
Acknowledgements
This work was supported by the EEC Contract Biomed/H4 CT95-0789, and by the Italian Consiglio Nazionale delle Ricerche.
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