The role of attention in human motor resonance

Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, exp...

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Published inPloS one Vol. 12; no. 5; p. e0177457
Main Authors Puglisi, Guglielmo, Leonetti, Antonella, Landau, Ayelet, Fornia, Luca, Cerri, Gabriella, Borroni, Paola
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 16.05.2017
Public Library of Science (PLoS)
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Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0177457

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Abstract Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, explored in different subject groups: in the first explicit condition, subjects were asked to observe a rhythmic hand flexion-extension movement performed live in front of them. In two other conditions subjects had to monitor the activity of a LED light mounted on the oscillating hand. The hand was clearly visible but it was not the focus of subjects' attention: in the semi-implicit condition hand movement was relevant to task completion, while in the implicit condition it was irrelevant. In a fourth, baseline, condition subjects observed the rhythmic oscillation of a metal platform. Motor resonance was measured with the H-reflex technique as the excitability modulation of cortico-spinal motorneurons driving a hand flexor muscle. As expected, a normal resonant response developed in the explicit condition, and no resonant response in the baseline condition. Resonant responses also developed in both semi-implicit and implicit conditions and, surprisingly, were not different from each other, indicating that viewing an action is, per se, a powerful stimulus for the action observation network, even when it is not the primary focus of subjects' attention and even when irrelevant to the task. However, the amplitude of these responses was much reduced compared to the explicit condition, and the phase-lock between the time courses of observed movement and resonant motor program was lost. In conclusion, different parameters of the response were differently affected by subtraction of attentional resources with respect to the explicit condition: time course and muscle selection were preserved while the activation of motor circuits resulted in much reduced amplitude and lost its kinematic specificity.
AbstractList Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, explored in different subject groups: in the first explicit condition, subjects were asked to observe a rhythmic hand flexion-extension movement performed live in front of them. In two other conditions subjects had to monitor the activity of a LED light mounted on the oscillating hand. The hand was clearly visible but it was not the focus of subjects' attention: in the semi-implicit condition hand movement was relevant to task completion, while in the implicit condition it was irrelevant. In a fourth, baseline, condition subjects observed the rhythmic oscillation of a metal platform. Motor resonance was measured with the H-reflex technique as the excitability modulation of cortico-spinal motorneurons driving a hand flexor muscle. As expected, a normal resonant response developed in the explicit condition, and no resonant response in the baseline condition. Resonant responses also developed in both semi-implicit and implicit conditions and, surprisingly, were not different from each other, indicating that viewing an action is, per se, a powerful stimulus for the action observation network, even when it is not the primary focus of subjects' attention and even when irrelevant to the task. However, the amplitude of these responses was much reduced compared to the explicit condition, and the phase-lock between the time courses of observed movement and resonant motor program was lost. In conclusion, different parameters of the response were differently affected by subtraction of attentional resources with respect to the explicit condition: time course and muscle selection were preserved while the activation of motor circuits resulted in much reduced amplitude and lost its kinematic specificity.
Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, explored in different subject groups: in the first explicit condition, subjects were asked to observe a rhythmic hand flexion-extension movement performed live in front of them. In two other conditions subjects had to monitor the activity of a LED light mounted on the oscillating hand. The hand was clearly visible but it was not the focus of subjects' attention: in the semi-implicit condition hand movement was relevant to task completion, while in the implicit condition it was irrelevant. In a fourth, baseline, condition subjects observed the rhythmic oscillation of a metal platform. Motor resonance was measured with the H-reflex technique as the excitability modulation of cortico-spinal motorneurons driving a hand flexor muscle. As expected, a normal resonant response developed in the explicit condition, and no resonant response in the baseline condition. Resonant responses also developed in both semi-implicit and implicit conditions and, surprisingly, were not different from each other, indicating that viewing an action is, per se, a powerful stimulus for the action observation network, even when it is not the primary focus of subjects' attention and even when irrelevant to the task. However, the amplitude of these responses was much reduced compared to the explicit condition, and the phase-lock between the time courses of observed movement and resonant motor program was lost. In conclusion, different parameters of the response were differently affected by subtraction of attentional resources with respect to the explicit condition: time course and muscle selection were preserved while the activation of motor circuits resulted in much reduced amplitude and lost its kinematic specificity.Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, explored in different subject groups: in the first explicit condition, subjects were asked to observe a rhythmic hand flexion-extension movement performed live in front of them. In two other conditions subjects had to monitor the activity of a LED light mounted on the oscillating hand. The hand was clearly visible but it was not the focus of subjects' attention: in the semi-implicit condition hand movement was relevant to task completion, while in the implicit condition it was irrelevant. In a fourth, baseline, condition subjects observed the rhythmic oscillation of a metal platform. Motor resonance was measured with the H-reflex technique as the excitability modulation of cortico-spinal motorneurons driving a hand flexor muscle. As expected, a normal resonant response developed in the explicit condition, and no resonant response in the baseline condition. Resonant responses also developed in both semi-implicit and implicit conditions and, surprisingly, were not different from each other, indicating that viewing an action is, per se, a powerful stimulus for the action observation network, even when it is not the primary focus of subjects' attention and even when irrelevant to the task. However, the amplitude of these responses was much reduced compared to the explicit condition, and the phase-lock between the time courses of observed movement and resonant motor program was lost. In conclusion, different parameters of the response were differently affected by subtraction of attentional resources with respect to the explicit condition: time course and muscle selection were preserved while the activation of motor circuits resulted in much reduced amplitude and lost its kinematic specificity.
Audience Academic
Author Landau, Ayelet
Cerri, Gabriella
Borroni, Paola
Fornia, Luca
Puglisi, Guglielmo
Leonetti, Antonella
AuthorAffiliation 2 Department of Medical Biotechnology and Translational Medicine, University of Milano, Medical School, Milan, Italy
4 Humanitas Clinical and Research Center, Rozzano, Italy
3 Department of Psychology & Department of Cognitive Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
1 Department of Health Sciences, University of Milano, Medical School, Milan, Italy
University of Bologna, ITALY
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– name: 4 Humanitas Clinical and Research Center, Rozzano, Italy
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  surname: Puglisi
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  surname: Leonetti
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28510605$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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2017 Puglisi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Conceptualization: GC PB.Data curation: GP A. Leonetti.Formal analysis: GP A. Leonetti A. Landau LF.Funding acquisition: PB.Investigation: GP A. Leonetti.Methodology: A. Landau GC PB.Project administration: PB.Supervision: PB.Visualization: GP A. Leonetti LF.Writing – original draft: GP PB.Writing – review & editing: A. Leonetti A. Landau LF GC PB.
Competing Interests: The authors have declared that no competing interests exist.
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Snippet Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor...
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StartPage e0177457
SubjectTerms Adult
Attention
Biology and Life Sciences
Biotechnology
Brain research
Circuits
Cognition & reasoning
Cortex (motor)
Evoked Potentials, Motor
Excitability
Female
H-Reflex
Hand
Health sciences
Humans
Light emitting diodes
Male
Medical schools
Medicine and Health Sciences
Motor cortex
Motor Cortex - physiology
Motor neurons
Motor task performance
Muscle, Skeletal - physiology
Neurons
Neurophysiology
Physical Sciences
Psychomotor Performance
Resonance
Rhythms
Social Sciences
Studies
Subtraction
Young Adult
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Title The role of attention in human motor resonance
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