Laila Craighero

Corticospinal excitability is specifically modulated by motor imagery : a magnetic stimulation study

Transcranial magnetic stimulation (TMS) was used to investigate whether the excitability of the corticospinal system is selectively affected by motor imagery. To this purpose, we performed two experiments. In the first one we recorded motor evoked potentials from right hand and arm muscles during mental simulation of flexion/extension movements of both distal and proximal joints. In the second experiment we applied magnetic stimulation to the right and the left motor cortex of subjects while they were imagining opening or closing their right or their left hand. Motor evoked potentials (MEPs) were recorded from a hand muscle contralateral to the stimulated cortex. The results demonstrated that the excitability pattern during motor imagery dynamically mimics that occurring during movement execution. In addition, while magnetic stimulation of the left motor cortex revealed increased corticospinal excitability when subjects imagined ipsilateral as well as contralateral hand movements, the stimulation of the right motor cortex revealed a facilitatory effect induced by imagery of contralateral hand movements only. In conclusion, motor imagery is a high level process, which, however, manifests itself in the activation of those same cortical circuits that are normally involved in movement execution.

Hand action preparation influences the responses to hand pictures

The relations between stimuli triggering a hand grasping movement and the subsequent action were studied in normal human participants. Participants were instructed to prepare to grasp a bar, oriented either clockwise or counterclockwise, and to grasp it as fast as possible on presentation of a visual stimulus with their right hand. The visual stimuli were pictures of the right hand as seen in a mirror. In Experiment 1, they represented the mirror image of the hand final posture as achieved in grasping the bar oriented either clockwise or counterclockwise. In Experiment 2, in addition to the pictures of Experiment 1, another two pictures, obtained rotating the hands represented in the previous ones of 90 degrees, were also used. Both experiments showed that the reaction times were faster when there was a similarity between hand position as depicted in the triggering visual stimulus and the grasping hand final position, the fastest responses being those where this similarity was the closest. In addition, Experiment 2 showed that reaction times to not rotated stimuli were faster than reaction times to the rotated stimuli, thus excluding a simple stimulus-response compatibility explanation of the findings. The data are interpreted as behavioral evidence that there is a close link between specific visual stimuli and specific motor actions. A neurophysiological model for this visuo-motor link is presented.

Broca's area in language, action, and music

The work of Paul Broca has been of pivotal importance in the localization of some higher cognitive brain functions. He first reported that lesions to the caudal part of the inferior frontal gyrus were associated with expressive deficits. Although most of his claims are still true today, the emergence of novel techniques as well as the use of comparative analyses prompts modern research for a revision of the role played by Brocas area. Here we review current research showing that the inferior frontal gyrus and the ventral premotor cortex are activated for tasks other than language production. Specifically, a growing number of studies report the involvement of these two regions in language comprehension, action execution and observation, and music execution and listening. Recently, the critical involvement of the same areas in representing abstract hierarchical structures has also been demonstrated. Indeed, language, action, and music share a common syntactic‐like structure. We propose that these areas are tuned to detect and represent complex hierarchical dependencies, regardless of modality and use. We speculate that this capacity evolved from motor and premotor functions associated with action execution and understanding, such as those characterizing the mirror‐neuron system.

Modulation of spinal excitability during observation of hand actions in humans.

There is growing evidence that observation of actions performed by other individuals activates observers cortical motor areas. This matching of observed actions on the observers motor repertoire could be at the basis of action recognition. Here we investigated if action observation, in addition to cortical motor areas, involves also low level motor structures mimicking the observed actions as if they were performed by the observer. Spinal cord excitability was tested by eliciting the H‐reflex in a finger flexor muscle (flexor digitorum superficialis) in humans looking at goal‐directed hand actions presented on a TV screen. We found that, in the absence of any detectable muscle activity, there was in the observers a significant modulation of the monosynaptic reflex size, specifically related to the different phases of the observed movement. The recorded H‐reflex rapidly increased in size during hand opening, it was depressed during hand closing and quickly recovered during object lifting. This modulation pattern is, however, opposite to that occurring when the recorded muscles are actually executing the observed action [Lemon et al. (1995) J. Neurosci., 15, 6145–56]. Considering that, when investigated at cortical level the modulation pattern of corticospinal excitability replicates the observed movements [Fadiga et al. (1995) J. Neurophysiol., 73, 2608–2611], this spinal ‘inverted mirror’ behaviour might be finalised to prevent the overt replica of the seen action.

Encoding of human action in Broca's area.

Brocas area has been considered, for over a century, as the brain centre responsible for speech production. Modern neuroimaging and neuropsychological evidence have suggested a wider functional role is played by this area. In addition to the evidence that it is involved in syntactical analysis, mathematical calculation and music processing, it has recently been shown that Brocas area may play some role in language comprehension and, more generally, in understanding actions of other individuals. As shown by functional magnetic resonance imaging, Brocas area is one of the cortical areas activated by hand/mouth action observation and it has been proposed that it may form a crucial node of a human mirror-neuron system. If, on the one hand, neuroimaging studies use a correlational approach which cannot offer a final proof for such claims, available neuropsychological data fail to offer a conclusive demonstration for two main reasons: (i) they use tasks taxing both language and action systems; and (ii) they rarely consider the possibility that Brocas aphasics may also be affected by some form of apraxia. We administered a novel action comprehension test--with almost no linguistic requirements--on selected frontal aphasic patients lacking apraxic symptoms. Patients, as well as matched controls, were shown short movies of human actions or of physical events. Their task consisted of ordering, in a temporal sequence, four pictures taken from each movie and randomly presented on the computer screen. Patients performance showed a specific dissociation in their ability to re-order pictures of human actions (impaired) with respect to physical events (spared). Our study provides a demonstration that frontal aphasics, not affected by apraxia, are specifically impaired in their capability to correctly encode observed human actions.

Evidence for visuomotor priming effect

‘WHILE seated, the patient took a glass, gave it to the examiner and then picked up a jug. He poured water into the glass and, having put down the jug, took the glass …’. This compulsive behaviour, described by Lhermitte in patients with frontal lobe lesions, is an example of how, without any internal motivation, visual stimuli may impel a patient to act and ‘grasp the objects presented and use them’. We investigated whether this behaviour is a pathological manifestation of a normal, automatic object to action transformation. To test this, we primed normal subjects, while ready to execute a grasping movement, by visually presenting them with drawings irrelevant to the task to be executed. Drawings visually congruent with the object to be grasped markedly reduced the reaction time for grasping. These data represent the first evidence for the existence of a visuomotor priming. Seeing an object facilitates an action congruent with the visual properties of that object.

Effects of spatial attention on directional manual and ocular responses

Abstract The aim of the present study was to investigate how spatial attention influences directional manual and saccadic reaction times. Two experiments were carried out. In experiment 1 subjects were instructed to perform pointing responses toward targets that were located either in the same or the opposite hemifield with respect to the hemifield in which an imperative stimulus was presented. In experiment 2, they were instructed to make saccadic or pointing responses. The direction of the responses was indicated by the shape of the imperative stimulus. Reaction time (RT), movement time, and, in experiment 2, saccadic trajectory were measured. The imperative stimulus location was either cued (endogenous attention) or uncued. In the latter case the imperative stimulus presentation attracted attention (exogenous attention). The main results of the experiments were the following: First, exogenous attention markedly decreased the RTs when the required movement was directed toward the imperative stimulus location. This directional effect was much stronger for pointing than for ocular responses. Second, endogenously allocated attention did not influence differentially RTs of pointing responses directed toward or away the attended hemifield. In contrast, endogenous attention markedly favored the saccadic responses when made away from the cued hemifield. Third, regardless of cueing, the direction of movement affected both pointing and saccadic reaction times. Saccadic reaction times were faster when the required movement was directed upward, while manual reaction times were faster when the movement was directed downward. Fourth, lateralized spatial attention deviated the trajectory of the saccades contralateral to the attention location. This pattern of results supports the notion that spatial attention depends on the activation of the same sensorimotor circuits that program actions in space.

Electrophysiology of action representation.

We continuously act on objects, on other individuals, and on ourselves, and actions represent the only way we have to manifest our own desires and goals. In the last two decades, electrophysiological experiments have demonstrated that actions are stored in the brain according to a goal-related organization. The authors review a series of experimental data showing that this “vocabulary of motor schemata” could also be used for non–strictly motor purposes. In the first section, they present data from monkey experiments describing the functional properties of inferior premotor cortex and, in more detail, the properties of visuomotor neurons responding to objects and others’ actions observation (mirror neurons). In the second section, human data are reviewed, with particular regard to electrophysiological experiments aiming to investigate how action representations are stored and addressed. The specific facilitatory effect of motor imagery, action/object observation, and speech listening on motor excitability shown by these experiments provides strong evidence that the motor system is constantly involved whenever the idea of an action is evoked.

Spatial attention-determined modifications in saccade trajectories.

Normal subjects were required to make horizontal or vertical saccades at the presentation of visual or acoustic imperative stimuli. The locations of visual imperative stimuli were orthogonal to the required saccade. Before stimulus presentation the subjects were cued about its location and instructed to allocate attention to it without moving the eyes. The main aim of the experiment was to establish whether the trajectory of horizontal saccades would be modified by spatial attention. The results showed that, with respect to the condition in which attention was on the horizontal meridian, the allocation of attention to the upper hemifield determined a downward saccade deviation, while the allocation to the lower hemifield determined an opposite deviation. The data strongly support the view that spatial attention and saccade programming share the same neural substrates.

Force requirements of observed object lifting are encoded by the observer’s motor system: a TMS study

Several transcranial magnetic stimulation (TMS) studies have reported facilitation of the primary motor cortex (M1) during the mere observation of actions. This facilitation was shown to be highly congruent, in terms of somatotopy, with the observed action, even at the level of single muscles. With the present study, we investigated whether this muscle‐specific facilitation of the observer’s motor system reflects the degree of muscular force that is exerted in an observed action. Two separate TMS experiments are reported in which corticospinal excitability was measured in the hand area of M1 while subjects observed the lifting of objects of different weights. The type of action ‘grasping‐and‐lifting‐the‐object’ was always identical, but the grip force varied according to the object’s weight. In accordance to previous findings, excitability of M1 was shown to modulate in a muscle‐specific way, such that only the cortical representation areas in M1 that control the specific muscles used in the observed lifting action became increasingly facilitated. Moreover, muscle‐specific M1 facilitation was shown to modulate to the force requirements of the observed actions, such that M1 excitability was considerably higher when observing heavy object lifting compared with light object lifting. Overall, these results indicate that different levels of observed grip force are mirrored onto the observer’s motor system in a highly muscle‐specific manner. The measured force‐dependent modulations of corticospinal excitability in M1 are hypothesized to be functionally relevant for scaling the observed grip force in the observer’s own motor system. In turn, this mechanism may contribute, at least partly, to the observer’s ability to infer the weight of the lifted object.