Literature DB >> 34862188

Feeling of Ownership over an Embodied Avatar's Hand Brings About Fast Changes of Fronto-Parietal Cortical Dynamics.

Elias Paolo Casula1,2, Gaetano Tieri3, Lorenzo Rocchi2,4, Rachele Pezzetta5, Michele Maiella6,7, Enea Francesco Pavone8, Salvatore Maria Aglioti9,10, Giacomo Koch6,11.   

Abstract

When we look at our body parts, we are immediately aware that they belong to us and we rarely doubt about the integrity, continuity, and sense of ownership of our body. Despite this certainty, immersive virtual reality (IVR) may lead to a strong feeling of embodiment over an artificial body part seen from a first-person perspective (1PP). Although such feeling of ownership (FO) has been described in different situations, it is not yet understood how this phenomenon is generated at neural level. To track the real-time brain dynamics associated with FO, we delivered transcranial magnetic stimuli over the hand region in the primary motor cortex (M1) and simultaneously recorded electroencephalography (EEG) in 19 healthy volunteers (11 male/8 female) watching IVR renderings of anatomically plausible (full-limb) versus implausible (hand disconnected from the forearm) virtual limbs. Our data show that embodying a virtual hand is temporally associated with a rapid drop of cortical activity of the onlookers' hand region in the M1 contralateral to the observed hand. Spatiotemporal analysis shows that embodying the avatar's hand is also associated with fast changes of activity within an interconnected fronto-parietal circuit ipsilateral to the brain stimulation. Specifically, an immediate reduction of connectivity with the premotor area is paralleled by an enhancement in the connectivity with the posterior parietal cortex (PPC) which is related to the strength of ownership illusion ratings and thus likely reflects conscious feelings of embodiment. Our results suggest that changes of bodily representations are underpinned by a dynamic cross talk within a highly-plastic, fronto-parietal network.SIGNIFICANCE STATEMENT Observing an avatar's body part from a first-person perspective (1PP) induces an illusory embodiment over it. What remains unknown are the cortical dynamics underpinning the embodiment of artificial agents. To shed light on the physiological mechanisms of embodiment we used a novel approach that combines noninvasive stimulation of the cortical motor-hand area and whole-scalp electroencephalographic (EEG) recordings in people observing an embodied artificial limb. We found that just before the illusion started, there is a decrease of activity of the motor-hand area accompanied by an increase of connectivity with the parietal region ipsilateral to the stimulation that reflects the ratings of the embodiment illusion. Our results suggest that changes of bodily representations are underpinned by a dynamic cross talk within a fronto-parietal circuit.
Copyright © 2022 the authors.

Entities:  

Keywords:  EEG; TMS; brain dynamics; embodiment

Mesh:

Year:  2021        PMID: 34862188      PMCID: PMC8805621          DOI: 10.1523/JNEUROSCI.0636-21.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  61 in total

1.  I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement.

Authors:  Eiichi Naito; Per E Roland; H Henrik Ehrsson
Journal:  Neuron       Date:  2002-12-05       Impact factor: 17.173

2.  Breakdown of cortical effective connectivity during sleep.

Authors:  Marcello Massimini; Fabio Ferrarelli; Reto Huber; Steve K Esser; Harpreet Singh; Giulio Tononi
Journal:  Science       Date:  2005-09-30       Impact factor: 47.728

3.  The role of the right temporo-parietal junction in maintaining a coherent sense of one's body.

Authors:  Manos Tsakiris; Marcello Costantini; Patrick Haggard
Journal:  Neuropsychologia       Date:  2008-06-14       Impact factor: 3.139

4.  Multiple nonprimary motor areas in the human cortex.

Authors:  G R Fink; R S Frackowiak; U Pietrzyk; R E Passingham
Journal:  J Neurophysiol       Date:  1997-04       Impact factor: 2.714

5.  Measuring the effects through time of the influence of visuomotor and visuotactile synchronous stimulation on a virtual body ownership illusion.

Authors:  Elena Kokkinara; Mel Slater
Journal:  Perception       Date:  2014       Impact factor: 1.490

Review 6.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research.

Authors:  Simone Rossi; Mark Hallett; Paolo M Rossini; Alvaro Pascual-Leone
Journal:  Clin Neurophysiol       Date:  2009-10-14       Impact factor: 3.708

7.  Hebbian and anti-Hebbian spike-timing-dependent plasticity of human cortico-cortical connections.

Authors:  Giacomo Koch; Viviana Ponzo; Francesco Di Lorenzo; Carlo Caltagirone; Domenica Veniero
Journal:  J Neurosci       Date:  2013-06-05       Impact factor: 6.167

8.  Test-retest reliability of transcranial magnetic stimulation EEG evoked potentials.

Authors:  Lewis J Kerwin; Corey J Keller; Wei Wu; Manjari Narayan; Amit Etkin
Journal:  Brain Stimul       Date:  2017-12-29       Impact factor: 8.955

9.  Transcranial Evoked Potentials Can Be Reliably Recorded with Active Electrodes.

Authors:  Marco Mancuso; Valerio Sveva; Alessandro Cruciani; Katlyn Brown; Jaime Ibáñez; Vishal Rawji; Elias Casula; Isabella Premoli; Sasha D'Ambrosio; John Rothwell; Lorenzo Rocchi
Journal:  Brain Sci       Date:  2021-01-22

10.  Illusory Obesity Triggers Body Dissatisfaction Responses in the Insula and Anterior Cingulate Cortex.

Authors:  Catherine Preston; H Henrik Ehrsson
Journal:  Cereb Cortex       Date:  2016-10-12       Impact factor: 5.357

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  5 in total

Review 1.  Motor awareness: a model based on neurological syndromes.

Authors:  Valentina Pacella; Valentina Moro
Journal:  Brain Struct Funct       Date:  2022-09-06       Impact factor: 3.748

2.  Multisensory Integration Dominates Hypnotisability and Expectations in the Rubber Hand Illusion.

Authors:  Mel Slater; H Henrik Ehrsson
Journal:  Front Hum Neurosci       Date:  2022-06-16       Impact factor: 3.473

3.  The effect of stimulation frequency on transcranial evoked potentials.

Authors:  Giorgio Leodori; Lorenzo Rocchi; Marco Mancuso; Maria Ilenia De Bartolo; Viola Baione; Matteo Costanzo; Daniele Belvisi; Antonella Conte; Giovanni Defazio; Alfredo Berardelli
Journal:  Transl Neurosci       Date:  2022-08-05       Impact factor: 1.264

4.  Causal Inference of Body Ownership in the Posterior Parietal Cortex.

Authors:  Marie Chancel; Heather Iriye; H Henrik Ehrsson
Journal:  J Neurosci       Date:  2022-08-08       Impact factor: 6.709

5.  Decreased Frontal Gamma Activity in Alzheimer Disease Patients.

Authors:  Elias P Casula; Maria C Pellicciari; Sonia Bonnì; Ilaria Borghi; Michele Maiella; Martina Assogna; Marilena Minei; Caterina Motta; Alessia D'Acunto; Francesco Porrazzini; Valentina Pezzopane; Lucia Mencarelli; Andrea Roncaioli; Lorenzo Rocchi; Danny A Spampinato; Carlo Caltagirone; Emiliano Santarnecchi; Alessandro Martorana; Giacomo Koch
Journal:  Ann Neurol       Date:  2022-07-07       Impact factor: 11.274

  5 in total

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