Robotically-induced hallucination triggers subtle changes in brain network transitions

The perception that someone is nearby, although nobody can be seen or heard, is called presence hallucination (PH). Being a frequent hallucination in patients with Parkinson's disease, it has been argued to be indicative of a more severe and rapidly advancing form of the disease, associated wit...

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Main Authors: Herberto Dhanis, Eva Blondiaux, Thomas Bolton, Nathan Faivre, Giulio Rognini, Dimitri Van De Ville, Olaf Blanke
Format: Article
Language:English
Published: Elsevier 2022-03-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921011332
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author Herberto Dhanis
Eva Blondiaux
Thomas Bolton
Nathan Faivre
Giulio Rognini
Dimitri Van De Ville
Olaf Blanke
author_facet Herberto Dhanis
Eva Blondiaux
Thomas Bolton
Nathan Faivre
Giulio Rognini
Dimitri Van De Ville
Olaf Blanke
author_sort Herberto Dhanis
collection DOAJ
description The perception that someone is nearby, although nobody can be seen or heard, is called presence hallucination (PH). Being a frequent hallucination in patients with Parkinson's disease, it has been argued to be indicative of a more severe and rapidly advancing form of the disease, associated with psychosis and cognitive decline. PH may also occur in healthy individuals and has recently been experimentally induced, in a controlled manner during fMRI, using MR-compatible robotics and sensorimotor stimulation. Previous neuroimaging correlates of such robot-induced PH, based on conventional time-averaged fMRI analysis, identified altered activity in the posterior superior temporal sulcus and inferior frontal gyrus in healthy individuals. However, no link with the strength of the robot-induced PH was observed, and such activations were also associated with other sensations induced by robotic stimulation. Here we leverage recent advances in dynamic functional connectivity, which have been applied to different psychiatric conditions, to decompose fMRI data during PH-induction into a set of co-activation patterns that are tracked over time, as to characterize their occupancies, durations, and transitions. Our results reveal that, when PH is induced, the identified brain patterns significantly and selectively increase their transition probabilities towards a specific brain pattern, centred on the posterior superior temporal sulcus, angular gyrus, dorso-lateral prefrontal cortex, and middle prefrontal cortex. This change is not observed in any other control conditions, nor is it observed in association with other sensations induced by robotic stimulation. The present findings describe the neural mechanisms of PH in healthy individuals and identify a specific disruption of the dynamics of network interactions, extending previously reported network dysfunctions in psychotic patients with hallucinations to an induced robot-controlled specific hallucination in healthy individuals.
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spelling doaj.art-07b21fb6df054f5db8da8158ddfa032a2022-12-21T23:44:59ZengElsevierNeuroImage1095-95722022-03-01248118862Robotically-induced hallucination triggers subtle changes in brain network transitionsHerberto Dhanis0Eva Blondiaux1Thomas Bolton2Nathan Faivre3Giulio Rognini4Dimitri Van De Ville5Olaf Blanke6Center for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne Switzerland; Department of Radiology and Medical Informatics, University of Geneva, Geneva SwitzerlandCenter for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandInstitute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne Switzerland; Department of Radiology and Medical Informatics, University of Geneva, Geneva SwitzerlandCenter for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; University. Grenoble Alpes, University Savoie Mont Blanc, CNRS, LPNC, 38000 Grenoble, FranceCenter for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandCenter for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne Switzerland; Department of Radiology and Medical Informatics, University of Geneva, Geneva Switzerland; Corresponding authors.Center for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Department of Clinical Neurosciences, University Hospital of Geneva, Geneva, Switzerland; Corresponding authors.The perception that someone is nearby, although nobody can be seen or heard, is called presence hallucination (PH). Being a frequent hallucination in patients with Parkinson's disease, it has been argued to be indicative of a more severe and rapidly advancing form of the disease, associated with psychosis and cognitive decline. PH may also occur in healthy individuals and has recently been experimentally induced, in a controlled manner during fMRI, using MR-compatible robotics and sensorimotor stimulation. Previous neuroimaging correlates of such robot-induced PH, based on conventional time-averaged fMRI analysis, identified altered activity in the posterior superior temporal sulcus and inferior frontal gyrus in healthy individuals. However, no link with the strength of the robot-induced PH was observed, and such activations were also associated with other sensations induced by robotic stimulation. Here we leverage recent advances in dynamic functional connectivity, which have been applied to different psychiatric conditions, to decompose fMRI data during PH-induction into a set of co-activation patterns that are tracked over time, as to characterize their occupancies, durations, and transitions. Our results reveal that, when PH is induced, the identified brain patterns significantly and selectively increase their transition probabilities towards a specific brain pattern, centred on the posterior superior temporal sulcus, angular gyrus, dorso-lateral prefrontal cortex, and middle prefrontal cortex. This change is not observed in any other control conditions, nor is it observed in association with other sensations induced by robotic stimulation. The present findings describe the neural mechanisms of PH in healthy individuals and identify a specific disruption of the dynamics of network interactions, extending previously reported network dysfunctions in psychotic patients with hallucinations to an induced robot-controlled specific hallucination in healthy individuals.http://www.sciencedirect.com/science/article/pii/S1053811921011332Presence HallucinationDynamic functional connectivityCo-activation pattern analysisNetwork interactionsPsychosisRobotics
spellingShingle Herberto Dhanis
Eva Blondiaux
Thomas Bolton
Nathan Faivre
Giulio Rognini
Dimitri Van De Ville
Olaf Blanke
Robotically-induced hallucination triggers subtle changes in brain network transitions
NeuroImage
Presence Hallucination
Dynamic functional connectivity
Co-activation pattern analysis
Network interactions
Psychosis
Robotics
title Robotically-induced hallucination triggers subtle changes in brain network transitions
title_full Robotically-induced hallucination triggers subtle changes in brain network transitions
title_fullStr Robotically-induced hallucination triggers subtle changes in brain network transitions
title_full_unstemmed Robotically-induced hallucination triggers subtle changes in brain network transitions
title_short Robotically-induced hallucination triggers subtle changes in brain network transitions
title_sort robotically induced hallucination triggers subtle changes in brain network transitions
topic Presence Hallucination
Dynamic functional connectivity
Co-activation pattern analysis
Network interactions
Psychosis
Robotics
url http://www.sciencedirect.com/science/article/pii/S1053811921011332
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