Elsevier

Cognitive Brain Research

Volume 15, Issue 3, February 2003, Pages 296-307
Cognitive Brain Research

Research report
Premotor cortex in observing erroneous action: an fMRI study

https://doi.org/10.1016/S0926-6410(02)00201-XGet rights and content

Abstract

The lateral premotor cortex (PMC) is involved during action observation in monkeys and humans, reflecting a matching process between observed actions and their corresponding motor schemata. In the present study, functional magnetic resonance imaging (fMRI) was used to investigate if paying attention to the two observable action components, objects and movements, modulates premotor activation during the observation of actions. Participants were asked to classify presented movies as showing correct actions, erroneous actions, or senseless movements. Erroneous actions were incorrect either with regard to employed objects, or to performed movements. The experiment yielded two major results: (1) The ventrolateral premotor cortex (vPMC) and the anterior part of the intraparietal sulcus (aIPS) are strongly activated during the observation of actions in humans. Premotor activation was dominantly located within Brodmann Area (BA) 6, and sometimes extended into BA 44. (2) The presentation of object errors and movements errors allowed to disentangle brain activations corresponding to the analysis of movements and objects in observed actions. Left premotor areas were more involved in the analysis of objects, whereas right premotor areas were dominant in the analysis of movements. It is suggested that the analysis of categorical information, like objects, and that of coordinate information, like movements, are pronounced in different hemispheres.

Introduction

How do we recognize others subjects’ actions? It is suggested that when we observe actions, their corresponding action schemata are triggered, including a ‘goodness-to-fit’ evaluation between the observed action and the triggered action schema [44], [46]. An action schema can be described on two levels, the goal of an action and its implementation [3], the latter of which can be defined by the actors’ movements and involved objects. Since the goal itself is not observable, the triggering of an action schema within the observing subject is necessarily based on at least one of the two observable components of implementation, i.e., objects and movements [7], [13], [14], [25].

Regarding cortical areas that are involved in action observation, research in humans [9], [26] and monkeys [21], [38], [45] indicates an outstanding role of the PMC. According to Rizzolatti and coworkers [44], in monkeys this cortex is a store of motor schemata. It responds whenever an observed action triggers a stored motor schema, and possibly also when both are subsequently subjected to a matching process. However, it remains unclear if observed objects and observed movements are processed differently within the PMC. The aim of our study was to clarify this question in the human PMC, using whole-brain fMRI.

We set out to dissociate both components of observed actions by manipulating objects and movements respectively. Subjects were scanned while observing actions and action slips, i.e., actions in which the implementation impedes the goal achievement [52]. Two types of action slips were employed. By violating the choice of an object, we realized actions with action-inappropriate objects (object errors). By violating a movement, we realized actions with action-inappropriate movements (movement errors). In clinical research, these two error types are also classified as ‘substitutional action slips’ and ‘qualitative action slips’, respectively [51]. In case that object-related observations and movement-related observations were processed differently within PMC, we expected these two types of errors to yield significantly different premotor activations.

Section snippets

Participants

Twelve healthy right-handed students (five female and seven male, aged 20–29 years, mean age 23.3) participated in the study. All had normal or corrected-to-normal vision. Participants gave written consent prior to testing. The experimental standards were approved by the local ethics committee of the University of Leipzig.

Stimuli and procedure

Movies were presented that showed either correct actions, actions characterized by object errors, actions characterized by movement errors, or aimless object manipulations

Behavioral performance

Behavioral performance was assessed by error rates and by reaction times of correct responses. A repeated measures ANOVA with the factor CONDITION (correct action, object error, movement error and baseline) indicated a main effect for error rates (F(3,33)=14.6, P<0.0001) and reaction times (F(3,33)=32.44, P<0.0001) (Fig. 2). Single t-tests with a Bonferoni α-level correction revealed that, compared to the classification of correct actions and erroneous actions, the movement classification was

Discussion

The present study investigated whether the observable components of action, i.e., employed objects and performed movements, are processed differently within the PMC. To this end, each component was manipulated distinctly in an error detection paradigm. Our findings revealed vPMC activation during the observation of correct actions, and during the observation of both movement-related and object-related violations, relative to baseline. However, conditions correct action and movement error

Conclusion

The present findings support the view that the vPMC (BA 6) and its parietal input zone are crucial for the observation of actions in humans. Moreover, we demonstrated that by attracting attention to either objects or to movements in action observation it is possible to examine how different components of this premotor-parietal network within each hemisphere contribute to action analysis.

Acknowledgements

We thank Marcel Brass, Christian Fiebach, Andrea Gast-Sandmann, Sonja Lattner, Stefan Pollmann, Markus Ullsperger and Stefan Zysset for helpful comments on the manuscript and technical support, and Volker Bosch, Gabriele Lohmann and Karsten Müller for support in statistical analysis.

References (56)

  • E. Phelps et al.

    Hemispheric differences in mnemonic processing: the effects of left hemisphere interpretation

    Neuropsychologia

    (1992)
  • A.M. Proverbio et al.

    Electrophysiological evidence of a perceptual precedence of global versus local visual information

    Cogn. Brain Res.

    (1998)
  • G. Rizzolatti et al.

    Language within our grasp

    Trends Neurosci.

    (1998)
  • R.I. Schubotz et al.

    Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed

    Cogn. Brain Res.

    (2001)
  • M. Vitkovitch et al.

    Visual field differences in an object decision task

    Brain Cogn.

    (1992)
  • K.J. Worsley et al.

    Analysis of fMRI time-series revisited-again

    NeuroImage

    (1995)
  • E. Zarahn et al.

    Empirical analysis of BOLD fMRI statistics. I. Spatially smoothed data collected under null-hypothesis conditions

    NeuroImage

    (1997)
  • K. Amunts et al.

    Broca’s region revisited: cytoarchitecture and intersubject variability

    J. Comp. Neurol.

    (1999)
  • M.A. Arbib

    Perceptual structures and distributed motor control

  • F. Binkosfki et al.

    Human anterior intraparietal area subserves prehension

    Neurology

    (1998)
  • F. Binkosfki et al.

    A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study

    Eur. J. Neurosci.

    (1999)
  • F. Binkosfki et al.

    A parieto-premotor network for object manipulation: evidence from neuroimaging

    Exp. Brain Res.

    (1999)
  • E. Bonda et al.

    Specific involvement of human parietal systems and the amygdala in the perception of biological motion

    J. Neurosci.

    (1996)
  • V. Bosch

    Statistical analysis of multi-subject fMRI data: the assessment of focal activations

    J. Magn. Reson. Imaging.

    (2000)
  • B. Buccino et al.

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

    Eur. J. Neurosci.

    (2001)
  • D. Caplan et al.

    Activation of Broca’s areas by syntactic processing under conditions of concurrent articulation

    Hum. Brain Mapp.

    (2000)
  • J. Decety et al.

    Brain activity during observation of actions. Influence of action content and subject’s strategy

    Brain

    (1997)
  • W.H. Dittrich

    Action categories and the perception of biological motion

    Perception

    (1993)
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