Robot-induced hallucinations in Parkinson's disease depend on altered sensorimotor processing in fronto-temporal network.

Journal: Science translational medicine
Published Date: Apr 28, 2021

Abstract

Hallucinations in Parkinson's disease (PD) are disturbing and frequent non-motor symptoms and constitute a major risk factor for psychosis and dementia. We report a robotics-based approach applying conflicting sensorimotor stimulation, enabling the induction of presence hallucinations (PHs) and the characterization of a subgroup of patients with PD with enhanced sensitivity for conflicting sensorimotor stimulation and robot-induced PH. We next identify the fronto-temporal network of PH by combining MR-compatible robotics (and sensorimotor stimulation in healthy participants) and lesion network mapping (neurological patients without PD). This PH-network was selectively disrupted in an additional and independent cohort of patients with PD, predicted the presence of symptomatic PH, and associated with cognitive decline. These robotics-neuroimaging findings extend existing sensorimotor hallucination models to PD and reveal the pathological cortical sensorimotor processes of PH in PD, potentially indicating a more severe form of PD that has been associated with psychosis and cognitive decline.

Authors

  • Fosco Bernasconi
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Eva Blondiaux
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Jevita Potheegadoo
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Giedre Stripeikyte
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Javier Pagonabarraga
    Movement Disorders Unit, Neurology Department, Sant Pau Hospital, 08041 Barcelona, Spain.
  • Helena Bejr-Kasem
    Movement Disorders Unit, Neurology Department, Sant Pau Hospital, 08041 Barcelona, Spain.
  • Michela Bassolino
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Michel Akselrod
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Saul Martinez-Horta
    Movement Disorders Unit, Neurology Department, Sant Pau Hospital, 08041 Barcelona, Spain.
  • Frederic Sampedro
    Movement Disorders Unit, Neurology Department, Sant Pau Hospital, 08041 Barcelona, Spain.
  • Masayuki Hara
    Graduate School of Science and Engineering, Saitama University, 338-8570 Saitama, Japan.
  • Judit Horvath
    Department of Neurology, Geneva University Hospitals, 1205 Geneva, Switzerland.
  • Matteo Franza
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Stéphanie Konik
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Matthieu Bereau
    Department of Neurology, Geneva University Hospitals, 1205 Geneva, Switzerland.
  • Joseph-André Ghika
    Department of Neurology, Hôpital du Valais, 1951 Sion, Switzerland.
  • Pierre R Burkhard
    Division of Neurology, Geneva University Hospitals, Geneva, Switzerland.
  • Dimitri Van De Ville
    Neuro-X Institute, Ecole Polytechnique Fédérale De Lausanne (EPFL), Geneva, Switzerland.
  • Nathan Faivre
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Giulio Rognini
    Center for Neuroprosthetics, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Cognitive Neuroscience, Brain Mind Institute, Faculty of Life Sciences, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Robotic Systems, School of Engineering, Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland. Electronic address: giulio.rognini@epfl.ch.
  • Paul Krack
    Department of Neurology, Inselspital, University Hospital and University of Bern, 3010 Bern, Switzerland.
  • Jaime Kulisevsky
    Movement Disorders Unit, Neurology Department, Sant Pau Hospital, Barcelona, Spain; Institut d'Investigacions Biomédiques Sant Pau (IIB-Sant Pau), Barcelona, Spain; Centro de Investigación en Red-Enfermedades Neurodegenerativas (CIBERNED), Barcelona, Spain; Universitat Autónoma de Barcelona (U.A.B.), Barcelona, Spain.
  • Olaf Blanke
    Center for Neuroprosthetics, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Cognitive Neuroscience, Brain Mind Institute, Faculty of Life Sciences, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Department of Neurology, University Hospital of Geneva, Geneva, Switzerland. Electronic address: olaf.blanke@epfl.ch.

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