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Sensorimotor mu rhythm during action observation changes across the lifespan independently from social cognitive processes.

ABSTRACT: The observation of actions performed by another person activates parts of the brain as if the observer were performing that action, referred to as the 'mirror system'. Very little is currently known about the developmental trajectory of the mirror system and related social cognitive processes. This experimental study sought to explore the modulation of the sensorimotor mu rhythm during action observation using EEG measures, and how these may relate to social cognitive abilities across the lifespan, from late childhood through to old age. Three-hundred and one participants aged 10- to 86-years-old completed an action observation EEG task and three additional explicit measures of social cognition. As predicted, findings show enhanced sensorimotor alpha and beta desynchronization during hand action observation as compared to static hand observation. Overall, our findings indicate that the reactivity of the sensorimotor mu rhythm to the observation of others' actions increases throughout the lifespan, independently from social cognitive processes.

SUBMITTER: Brunsdon VEA

PROVIDER: S-EPMC6688050 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Sensorimotor mu rhythm during action observation changes across the lifespan independently from social cognitive processes.

Brunsdon Victoria E A VEA Bradford Elisabeth E F EEF Ferguson Heather J HJ

Developmental cognitive neuroscience 20190517

The observation of actions performed by another person activates parts of the brain as if the observer were performing that action, referred to as the 'mirror system'. Very little is currently known about the developmental trajectory of the mirror system and related social cognitive processes. This experimental study sought to explore the modulation of the sensorimotor mu rhythm during action observation using EEG measures, and how these may relate to social cognitive abilities across the lifesp ...[more]

PMID: 31132663

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Project description:The alpha mu rhythm (8-13 Hz) has been considered to reflect mirror neuron activity because it is attenuated by both action observation and action execution. The putative link between mirror neuron system activity and the mu rhythm has been used to study the involvement of the mirror system in a wide range of socio-cognitive processes and clinical disorders. However, previous research has failed to convincingly demonstrate the specificity of the mu rhythm, meaning that it is unclear whether the mu rhythm reflects mirror neuron activity. It also remains unclear whether mu rhythm suppression during action observation reflects the processing of motor or tactile information. In an attempt to assess the validity of the mu rhythm as a measure of mirror neuron activity, we used crossmodal pattern classification to assess the specificity of EEG mu rhythm response to action varying in terms of action type (whole-hand or precision grip), concurrent tactile stimulation (stimulation or no stimulation), or object use (transitive or intransitive actions) in 20 human participants. The main results reveal that above-chance crossmodal classification of mu rhythm activity was obtained in the central channels for tactile stimulation and action transitivity but not for action type. Furthermore, traditional univariate analyses applied to the same data were insensitive to differences between conditions. By calling into question the relationship between mirror system activity and the mu rhythm, these results have important implications for the use and interpretation of mu rhythm activity.SIGNIFICANCE STATEMENT The central alpha mu rhythm oscillation is a widely used measure of the human mirror neuron system that has been used to make important claims concerning cognitive functioning in health and in disease. Here, we used a novel multivariate analytical approach to show that crossmodal EEG mu rhythm responses primarily index the somatosensory features of actions, suggesting that the mu rhythm is not a valid measure of mirror neuron activity. Results may lead to the revision of the conclusions of many previous studies using this measure, and to the transition toward a theory of mu rhythm function that is more consistent with current models of sensory processing in the self and in others.

Project description:Theta oscillations (4-8 Hz) provide an organizing principle of cognitive control, allowing goal-directed behavior. In adults, theta power over medial-frontal cortex (MFC) underlies conflict/error monitoring, whereas theta connectivity between MFC and lateral-frontal regions reflects cognitive control recruitment. However, prior work has not separated theta responses that occur before and immediately after a motor response, nor explained how medial-lateral connectivity drives different kinds of control behaviors. Theta's role during adolescence, a developmental window characterized by a motivation-control mismatch also remains unclear. As social observation is known to influence motivation, this might be a particularly important context for studying adolescent theta dynamics. Here, adolescents performed a flanker task alone or under social observation. Focusing first on the nonsocial context, we parsed cognitive control into dissociable subprocesses, illustrating how theta indexes distinct components of cognitive control working together dynamically to produce goal-directed behavior. We separated theta power immediately before/after motor responses, identifying behavioral links to conflict monitoring and error monitoring, respectively. MFC connectivity was separated before/after responses and behaviorally-linked to reactive and proactive control, respectively. Finally, distinct forms of post-error control were dissociated, based on connectivity with rostral/caudal frontal cortex. Social observation was found to exclusively upregulate theta measures indexing post-response error monitoring and proactive control, as opposed to conflict monitoring and reactive control. Linking adolescent cognitive control to theta oscillations provides a bridge between non-invasive recordings in humans and mechanistic studies of neural oscillations in animal models; links to social observation provide insight into the motivation-control interactions that occur during adolescence.

Dataset Information

Sensorimotor mu rhythm during action observation changes across the lifespan independently from social cognitive processes.

Publications

Sensorimotor mu rhythm during action observation changes across the lifespan independently from social cognitive processes.

Similar Datasets

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