Elsevier

Brain Research

Volume 1065, Issues 1–2, 14 December 2005, Pages 115-124
Brain Research

Research Report
Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement

https://doi.org/10.1016/j.brainres.2005.10.034Get rights and content

Abstract

The observation of a sinusoidal flexion–extension of the wrist was utilized to determine the continuous time course and phase relation between observed movement and its effects on the observer's motor pathways. While observing movements performed by others, the observers' cortical motor areas and spinal circuits were activated, reflecting the specific temporal and muscular pattern of the actual movement (motor resonance). H-reflexes and motor-evoked potentials (MEPs) were elicited, respectively, by electrical stimulation of the median nerve and magnetic stimulation of the appropriate cortical area, in the right forearm muscle Flexor Carpi Radialis (FCR) of subjects who were observing a 1-Hz cyclic oscillation of the right prone hand executed by a different person. Observation elicited a parallel cyclic excitability modulation of the observer's H-reflex and MEP responses with identical period as the observed movement. Modulation was phase advanced, as is muscle activation with respect to the real movement. The same results were obtained when the observed hand oscillation was executed with different frequency (1.6 Hz) and when the hands of mover and observer were supine. No motor resonance was elicited by observing the oscillation of a metal platform. The excitability modulation of MEPs simultaneously monitored in both antagonists of the observer's forearm (FCR and Extensor Carpi Radialis, ECR) was in almost perfect phase opposition, reflecting their natural reciprocal activation during the execution of a hand oscillation. These findings suggest that during observation, motor pathways are modulated subliminally reproducing with high temporal fidelity the motor commands needed to execute the observed movement.

Introduction

It has recently emerged from a number of studies that motor pathways are activated not only during the obvious task of producing voluntary movement but also during motor imagery [33] and during action observation [43], [44]. In particular, it has been proposed that during action observation, a “motor resonance”, so termed to emphasize the concord of neural activity between mover and observer, may be an important mechanism underlying the automatic understanding of actions performed by others and/or the imitative learning of some motor skills [18], [32], [42].

Single unit recordings from a cortical premotor area in the macaque monkey (F5) [13], [19] have disclosed neurons that produce a similar firing pattern when the monkey performs a goal-directed hand action and when it observes another monkey or a human experimenter perform a similar action (“mirror” neurons). Further experiments have revealed that the response of the mirror system is very robust, demonstrating that it concerns also goal-oriented actions performed with the mouth or foot [6], [17], [39], and that it is activated also in response to observed actions that are not completed in front of the monkey but have to be partly imagined by the animal [47] or that could just be inferred listening to recognizable sounds, causally linked to specific actions [36].

A corresponding observation/execution system has also been described in human observers by various techniques such as electro- and magnetoencephalography [10], [26], functional magnetic resonance [6], [7], [29], positron emission tomography [12], [24], [25], [42], all of which have documented the activation of cortical premotor and/or motor areas, during action observation tasks. These studies have confirmed that observation of a specific action can excite in the observer the same neural substrate necessary for the execution of that action. Differences between human and monkey observers have also emerged, such as, for example, the fact that for human subjects intransitive (not goal-directed) movements are also effective stimuli in evoking a motor resonant response [30], [37]. Utilizing transcranial magnetic stimulation (TMS), several authors have been able to investigate motor resonance in human subjects with higher spatial resolution, describing a specific subliminal activation in those muscles that the observer would have used if enacting the observed movement [16], [20], [21], [45]. With the H-reflex technique, Baldissera et al. [2] demonstrated that resonance phenomena are not confined to cortical structures but spread to modulate the excitability of spinal motoneurones. This study however showed that the excitability of the H-reflex evoked in a finger flexor muscle (Flexor Digitorum Superficialis, FDS) was depressed during the observation of fingers closing on an object, an unexpected result, given that all other evidence shows a consistent “mirror” activation of neural pathways in movers and observers. The apparent contradiction has been recently resolved, showing that, during the grasping movement, the FDS muscle, despite being a finger flexor, reaches its maximal activation during the hand opening phase [38], i.e., in accordance with maximal excitability of the H-reflex in observers. Indeed, a problem common to motor resonance studies to date has been the lack of an accurate temporal resolution of the correspondence between the observation of complex and prolonged movements and its modulatory effects in the observer.

In the present study, aimed at solving this problem, the hypothesis that a subliminal temporal pattern of muscle activation similar to that responsible for the actual movement might be produced during action observation was tested by using a simple, intransitive movement: the cyclic flexion–extension of the wrist. The excitability modulation induced in the observer's spinal and cortical motor pathways of two wrist muscles (FCR and ECR) was sampled with both H-reflexes and MEPs. By using the same sinusoidal function to fit both observed wrist oscillation and resonance effects on the observer's wrist motor circuits, we could describe a continuous time course of the two events and determine their precise phase relation.

Section snippets

Material and methods

Subjects gave informed written consent to all experiments, which were performed according to the Declaration of Helsinki and approved by the local ethics committee. Each experimental session involved two individuals sitting comfortably in front of each other, one performing a cyclic flexion–extension movement of the right hand around the wrist (mover) and the other observing such movement while not moving (observer, the true subject of the experiment).

Results

The first 2 series of experiments describe the changes of the H-reflex excitability in the resting FCR muscle induced by the observation of a cyclic wrist movement performed by a different subject. The time course of the H-reflex modulation in the observer's flexor muscle closely reproduces that of the mover's hand flexion (maximum H-reflex amplitude) and extension (minimum amplitude); this subliminar modulation is maintained irrespective of whether the hands are kept prone (downward flexion)

Discussion

Observation of movement executed by others elicits in specific motor pathways of the observer a “resonant” response with the same time course and muscular activation pattern as in the observed movement. This statement is supported by several converging results obtained in this study with different experimental approaches. Watching a sinusoidal flexion–extension of the wrist elicited a sinusoidal excitability modulation in the motor pathways of the observer's wrist muscles, measured as changes

Acknowledgments

This study was supported by grants from the “Ministero dell'Istruzione e dell'Università” and by the “Università degli Studi di Milano”.

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