Elsevier

Neuropsychologia

Volume 47, Issue 2, January 2009, Pages 415-422
Neuropsychologia

How are observed actions mapped to the observer’s motor system? Influence of posture and perspective

https://doi.org/10.1016/j.neuropsychologia.2008.09.012Get rights and content

Abstract

Previous studies using transcranial magnetic stimulation (TMS) have shown that during the observation of actions performed by others, the observer’s primary motor cortex (M1) becomes facilitated in a highly muscle specific fashion. Here, we used TMS to explore the effect of posture, perspective and body side on muscle specific facilitation of left M1. Subjects viewed video’s showing left and right hand extension (palm-down) movements from a first person or third person perspective with their hand posture either congruent (palm-down) or incongruent (palm-up) to the posture of the observed model.

Data indicated that facilitation of left M1 was substantially different for observing actions executed with the right (contralateral) or left (ipsilateral) hand. For right hand actions, facilitation of left M1 was shown to be highly specific to the muscle used in the observed action (‘intrinsic mapping’). During the observation of left hand stimuli, only half of the subjects displayed this muscle specific facilitation, whereas in the other half, M1 was facilitated according to the observed movement direction (‘extrinsic mapping’). Absolute effect magnitude was particularly high when right hand actions were observed from a first person perspective, whereas, for left hand actions, the third person perspective was more efficient. The degree of postural congruency between body parts of the observer and observed model only mildly influenced M1 facilitation. Since action observation is increasingly considered in rehabilitation therapies, the present findings may help identifying the most effective conditions for stimulating the motor system during action observation.

Introduction

In a socially dynamic world, basic understanding and imitation of others’ gestures and movements is fundamental to human communicative behaviour and observational learning. A neural circuitry that is associated with these cognitive functions has been discovered in the macaque brain (Di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). The cells of this circuitry, the so-called ‘mirror neurons’ have the striking property not only to fire when the monkey performs an action, but also when the monkey observes a similar action performed by someone else (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti & Craighero, 2004; Rizzolatti, Fadiga, Gallese, & Fogassi, 1996a).

A similar fronto-parietal ‘mirror neuron system’ has also been identified in the human brain (Buccino et al., 2001, Iacoboni et al., 1999, Rizzolatti et al., 1996b). With single-pulse transcranial magnetic stimulation (TMS), it was also shown that the observer’s motor system ‘resonates’ with the observed movements such that muscles involved in a certain action become facilitated by merely observing this action (Brighina, La Bua, Oliveri, Piazza, & Fierro, 2000; Fadiga, Craighero, & Olivier, 2005; Fadiga, Fogassi, Pavesi, & Rizzolatti, 1995; Gangitano, Mottaghy, & Pascual-Leone, 2001; Strafella & Paus, 2000). Recent research has shown that this resonating activity might provide a window into how the observed movement is mapped onto the observer’s body scheme (Lamm, Fischer, & Decety, 2007). In daily life, the actions of others are often observed in different ways, which can roughly be characterized according to three distinct dimensions. First, the presence or absence of postural congruency between the observer’s and actor’s physical state might influence the effectiveness of movement observation. For example, observing another person typing at a keyboard might induce more resonating activity when the observer’s hand is in pronation instead of supination. Second, peers can be perceived from different perspectives. Here, we will refer to an egocentric perspective (Ego) when the observed movement orientation corresponds to that of the observer (as if the action would be performed by the observer him/herself). In the allocentric perspective (Allo), the observed movement orientation is opposed to that of the observer (i.e., when an action is performed by another person facing the observer). Third, the observed action might exhibit congruency in terms of the observed body side (i.e., observing a right hand movement is anatomically congruent with the observer’s right but not left hand).

Action observation is increasingly considered in rehabilitation contexts (Buccino, Solodkin, & Small, 2006; Ertelt et al., 2007, Mulder, 2007, Pomeroy et al., 2005), such that a deeper understanding of the effects of body side, posture, and perspective is crucial for identifying the most effective conditions for stimulation of the motor system during action observation. Moreover, observational training programs in ergonomics and recreational contexts may also benefit from this knowledge.

Here, we aimed to explore the effects of these three factors, posture, perspective and body side, on muscular motor facilitation during action observation. For this purpose, TMS was used to measure the level of motor facilitation of the right flexor and extensor carpi radialis muscles (FCR/ECR) during the passive observation of several video clips showing simple extension movements of a model’s wrist. In a previous study, it was already established that this action observation paradigm is suited to reveal a coherent picture of muscle specific facilitation of the observer’s motor system, i.e., a stronger facilitation of the extensor muscle compared to the flexor as a result of extension movement observation (Alaerts, Swinnen, & Wenderoth, in press). Overall, we expected the general muscle specific facilitation response to be preserved, but its magnitude to vary as a function of posture, body side and perspective.

The effect of posture was assessed by varying the observer’s hand position from palm-down to palm-up, i.e., postures were congruent when extension movements were observed with palm-down posture, and incongruent for observation with palm-up posture. To assess the effect of the observer’s perspective, video clips were observed from either an egocentric or allocentric perspective. To assess the effect of body side, both left and right hand extension movements were shown. Since cortico-spinal excitability was measured only in right ECR and FCR muscles, body sides were congruent for observing right hand and incongruent for observing left hand movements.

We hypothesized that muscle specific facilitation is reduced: (i) when the postures of model and observer are incongruent, (ii) when the actions are observed from an allocentric as compared to egocentric perspective, and (iii) when ‘incongruent’ left hand actions are observed (Aziz-Zadeh, Maeda, Zaidel, Mazziotta, & Iacoboni, 2002). However, an alternative hypothesis is that left hand actions shown from an allocentric perspective are particularly beneficial in facilitating left M1, as suggested by a large body of behavioural work showing that mirror imitation is a more natural behaviour than anatomical imitation in many daily live tasks (Bekkering, Wohlschlager, & Gattis, 2000; Gleissner, Meltzoff, & Bekkering, 2000; Wapner & Cirillo, 1968).

Section snippets

Subjects

Participants were 4 male and 10 female university students (age range 20–28) without any known neuromuscular disorders. None were involved in neuroscience programs. All participants were right-handed, as assessed with the Edinburgh Handedness Questionnaire (Oldfield, 1971) and were naive about the purpose of the experiment. Written informed consent was obtained before the experiment and all subjects were screened for potential risk of adverse effects during TMS. The experimental procedure as

Results

Normalized MEP amplitudes recorded from the ECR and FCR are reported in Table 1 for each observation condition. The ANOVA revealed a two-way interaction of ‘Posture × Body side’ for the normMEPs recorded from the FCR [F(1,12) = 9.01, p = 0.01], which indicated that MEP responses of the FCR were higher for observing left hand actions with incongruent postures than with congruent postures. Overall, FCR excitability was low for observing right hands with either posture (Table 1). For the normMEPs

Discussion

The influence of posture, perspective, and body side on movement observation was investigated by means of a full factorial design. The analyses revealed substantial differences in the responses of the observers’ left M1 when right (contralateral) versus left (ipsilateral) hand actions were observed.

  • (1)

    When observing right hand actions, all subjects mapped the observed movements in a highly muscle specific way to their own body (intrinsic mapping). By contrast, when left hand actions were observed,

Summary and conclusions

The present study suggests that M1 of the left hemisphere responds to observing actions executed with the right (contralateral) or left (ipsilateral) hand. For right limb stimuli, activations in left M1 are highly specific to the muscle used in the observed action (‘intrinsic mapping’). During the observation of left limb stimuli, only part of the subjects display this muscle specific activation of left M1, whereas in others, primary motor cortex appears to resonate with respect to the observed

Acknowledgements

Support for this study was provided through grants from the Flanders Fund for Scientific Research (Projects G.0292.05 and G.0577.06). This work was also supported by Grant P6/29 from the Interuniversity Attraction Poles program of the Belgian federal government.

References (37)

  • L. Aziz-Zadeh et al.

    Lateralization of the human mirror neuron system

    Journal of Neuroscience

    (2006)
  • F. Baldissera et al.

    Modulation of spinal excitability during observation of hand actions in humans

    European Journal of Neuroscience

    (2001)
  • H. Bekkering et al.

    Imitation of gestures in children is goal-directed

    Quarterly Journal of Experimental Psychology Section A: Human Experimental Psychology

    (2000)
  • G. Buccino et al.

    Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study

    European Journal of Neuroscience

    (2001)
  • G. Buccino et al.

    Functions of the mirror neuron system: Implications for neurorehabilitation

    Cognitive and Behavioral Neurology

    (2006)
  • B. Calvo-Merino et al.

    Action observation and acquired motor skills: An fMRI study with expert dancers

    Cerebral Cortex

    (2005)
  • G. Di Pellegrino et al.

    Understanding motor events: A neurophysiological study

    Experimental Brain Research

    (1992)
  • L. Fadiga et al.

    Motor facilitation during action observation: A magnetic stimulation study

    Journal of Neurophysiology

    (1995)
  • Cited by (0)

    View full text