Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation
Introduction
Various experimental designs have been used in animals to investigate the mechanisms involved in the observation of motor actions. Monkey agranular frontal cortex has been used and may be functionally subdivided into several different areas [32]. Stimulation and recording experiments have been conducted on the ventral premotor cortex. These studies have shown various interesting properties of the F5 area, demonstrating that this area is involved in hand and mouth movements [13], [21], [28], [35]. Hand-related premotor neurons have been found to discharge selectively during goal-oriented movements such as grasping, manipulating, holding and tearing objects. In particular, some of them are specific for the type of hand grip [35]. A particular subset of F5 neurons, called “mirror neurons” on the basis of their properties, are activated by the observation of motor actions performed in front of the observer by another subject. Mirror neurons of the hand are activated by object-interactive movements and do not discharge with the same intensity during the presentation of hand actions mimicking the grasping of objects [11]. Premotor neurons were found to retrieve movements not only on the basis of stimulus characteristics, but also in relation to the meaning of the action observed [7]. An interesting theory about the derivation of the lateral verbal communication system in humans from a more ancient communication system based on hand and facial gestures has been proposed recently [36], thus shedding light on the importance of the recognition of movements and the possible role of an observation/execution matching system similar to the one present in the monkey premotor cortex.
While the substrate of activation in motor action is more detailed in animal models, the information in humans depends on neuroradiological findings. Electrophysiological and brain imaging studies have recently shown that a motor system dependent on action observation also exists in human subjects. Electroencephalographic (EEG) [29] and magneto-encephalographic studies [17] have shown that during action-viewing there is desynchronisation of cortical rhythms in the perirolandic derivations of the skull. Positron emission tomography (PET) [6], [15], [16], [37] and functional magnetic resonance (fMRI) [3] have demonstrated that observation of actions activates the cortex of the mid-temporal gyrus including that of the adjacent superior temporal sulcus (Broadmann area 21) and the caudal part of the left inferior frontal gyrus (Broadmann area 45). As in monkeys, the existence of a “mirror” system activated during action-viewing has been postulated in humans and probably plays an important role in movement imitation and recognition [12], [23]. Transcranial magnetic stimulation (TMS) has been used by several authors [4], [10], [39] to explore motor system modulation during observation of motor actions in human subjects. These investigators found facilitation of the amplitude of single-pulse motor evoked potentials (MEPs) of hand muscles during the observation of grasping actions [4], [10]. More recent studies have found a reduction in intracortical inhibition (ICI) and in intracortical facilitation (ICF) by paired magnetic stimulation during the observation of actions performed by another individual. Furthermore, this effect is specific to the muscle involved in the action observed. There have been no studies, however, exploring the effects produced by the observation of the subject’s own hand movements, whereas in previous tasks the subjects had to watch actions performed by the experimenter or by other individuals. Recently, a TMS study on self-recognition [24] has shown that neural substrates in the right hemisphere may selectively participate in processes linked to self-awareness and that a greater increase in motor excitability occurs during the observation of pictures containing elements of the subject’s own face or familiar faces than during the observation of unfamiliar ones. In addition, neuropsychological studies show that humans are poorly aware of their own movements and that they tend to mistake non-self-movements for their own [5], [22], [33].
We investigated the possible parallel activation of the motor system during self- and non-self-hand movement observation. Different control conditions were included in our examination such as motor imagery and the observation of moving geometric objects.
Section snippets
Subjects
Ten normal healthy subjects (five females and five males) aged from 21 to 33 years participated in the study. All subjects were right-handed and had normal or corrected-normal visual acuity. Informed consent was obtained before starting the procedure. The experimental design was discussed and accepted by the local ethical committee. All subjects were familiar with neurophysiological examinations. Two of the authors participated in the study as well.
Magnetic stimulation procedure
TMS was applied through a circular magnetic
Single-pulse TMS
MEPs evoked by a single magnetic pulse were significantly facilitated during self-MO, non-self-MO and MI (F4,36=5.81; P<0.05) compared to RC (see Fig. 1 and Table 1). No significant changes in mean MEP amplitude during object observation were observed compared to RC. No significant differences in mean MEP amplitude were observed between self-MO, non-self-MO and MI. No significant changes were observed in RMT during the self-MO, non-self-MO and MI conditions.
ICI
ICI was significantly reduced during
Discussion
The novel aspect of the study consists in the investigation of self-recognition of hand movements. The main finding worthy to note was that we detected an increase in MEP amplitude associated with a reduction in ICI during the observation of both self- and non-self-finger flexion in the FDS as compared to the rest condition. This may be interpreted in the light of previous neuropsychological studies [14], [25] regarding self- and non-self-MO.
No significant differences between motor excitability
References (42)
- et al.
Magnetic stimulation study during observation of motor tasks
Journal of the Neurological Sciences
(2000) - et al.
Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients
Cognition
(1997) - et al.
Mirror neurons and the simulation theory of mind-reading
Trends in Cognitive Sciences
(1998) - et al.
Beyond consciousness of external reality: a who system for consciousness of action and self-consciousness
Consciousness and Cognition
(1998) - et al.
Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery
Brain Research
(1997) - et al.
Crossed and direct effects of digital nerve stimulation on motor evoked potential: a study with magnetic stimulation
Electroencephalography and Clinical Neurophysiology
(1997) - et al.
Premotor cortex and the recognition of motor actions
Cognitive Brain Research
(1996) - et al.
Reversible changes of motor cortical outputs following immobilization of the upper limb
Electroencephalography and Clinical Neurophysiology
(1997) - et al.
Changes of intracortical inhibition during motor imagery in human subjects
Neuroscience Letters
(1999) - et al.
Modulation of spinal excitability during observation of hand actions in humans
European Journal of Neuroscience
(2001)
Topographic segregation for movement recognition in man. An fMRI-study
Abstracts—Society for Neuroscience
Brain activity during observation of actions. Influence of action content and subject’s strategy
Brain
Understanding motor events: a neurophysiological study
Experimental Brain Research
The origin of cortico-spinal projections from the premotor areas in the frontal lobe
The Journal of Neuroscience
Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study
Acta Neurologica Scandinavica
Motor facilitation during action observation: a magnetic stimulation study
Journal of Neurophysiology
Action recognition in the premotor cortex
Brain
Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements
Experimental Brain Research
Localization of grasp representation in humans by positron emission tomography. 2. Observation compared with imagination
Experimental Brain Research
Top-down effect of the strategy on the perception of biological motion: a PET investigation
Cognitive Neuropsychology
Action of human primary motor cortex during action observation: a neuromagnetic study
Proceedings of the National Academy of Sciences of the United States of America
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