Neuroscience robotics for controlled induction and real-time assessment of hallucinations

Fosco Bernasconi, Eva Blondiaux, Giulio Rognini, Herberto Dhanis, Laurent Jenni, Jevita Potheegadoo, Masayuki Hara, Olaf Blanke

Published: 2022-09-11 DOI: 10.1038/s41596-022-00737-z

Neuroscience Robotics

Hallucination Induction

Sensorimotor Stimulation

MRI-Compatible Robotics

Biomarker Identification

AI 解读

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2 and Figs. 1–3.

Reporting Summary

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Pearson, J. et al. Sensory dynamics of visual hallucinations in the normal population. eLife 5, e17072 (2016).
Tracy, D. K. & Shergill, S. S. Mechanisms underlying auditory hallucinations—understanding perception without stimulus. Brain Sci. 3, 642–669 (2013).
Corlett, P. R. et al. Hallucinations and strong priors. Trends Cogn. Sci. 23, 114–127 (2019).
Larøi, F. et al. An epidemiological study on the prevalence of hallucinations in a general-population sample: effects of age and sensory modality. Psychiatry Res. 272, 707–714 (2019).
Badcock, J. C., Dehon, H. & Larøi, F. Hallucinations in healthy older adults: an overview of the literature and perspectives for future research. Front. Psychol. 8, 1134 (2017).
Badcock, J. C. et al. Hallucinations in older adults: a practical review. Schizophr. Bull. 46, 1382–1395 (2020).
Ohayon, M. M. Prevalence of hallucinations and their pathological associations in the general population. Psychiatry Res. 97, 153–164 (2000).
Collerton, D., Perry, E. & McKeith, I. Why people see things that are not there: a novel perception and attention deficit model for recurrent complex visual hallucinations. Behav. Brain Sci. 28, 737–794 (2005).
Insel, T. R. Rethinking schizophrenia. Nature 468, 187–193 (2010).
Arnaoutoglou, N. A., O’Brien, J. T. & Underwood, B. R. Dementia with Lewy bodies—from scientific knowledge to clinical insights. Nat. Rev. Neurol. 15, 103–112 (2019).
Ffytche, D. H. et al. The psychosis spectrum in Parkinson disease. Nat. Rev. Neurol. 13, 81–95 (2017).
Millan, M. J. et al. Altering the course of schizophrenia: progress and perspectives. Nat. Rev. Drug Discov. 15, 485–515 (2016).
Llorca, P. M. et al. Hallucinations in schizophrenia and Parkinson’s disease: an analysis of sensory modalities involved and the repercussion on patients. Sci. Rep. 6, 38152 (2016).
Jaspers, K. Über leibhaftige Bewußtheiten (Bewußtheitstäuschungen), ein psychopathologisches Elementarsymptom. Z. Pathopsychol. 2, 150–161 (1913).
McKeith, I. G. et al. Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology 89, 88–100 (2017).
Buracchio, T., Arvanitakis, Z. & Gorbien, M. Dementia with Lewy bodies: current concepts. Dement. Geriatr. Cogn. Disord. 20, 306–320 (2005).
Walker, Z., Possin, K. L., Boeve, B. F. & Aarsland, D. Lewy body dementias. Lancet 386, 1683–1697 (2015).
Nagahama, Y. et al. Classification of psychotic symptoms in dementia with Lewy bodies. Am. J. Geriatr. Psychiatry 15, 961–967 (2007).
Eversfield, C. L. & Orton, L. D. Auditory and visual hallucination prevalence in Parkinson’s disease and dementia with Lewy bodies: a systematic review and meta-analysis. Psychol. Med. 49, 2342–2353 (2019).
Nicastro, N., Eger, A. F., Assal, F. & Garibotto, V. Feeling of presence in dementia with Lewy bodies is related to reduced left frontoparietal metabolism. Brain Imaging Behav. 14, 1199–1207 (2020).
Goetz, C. G., Fan, W., Leurgans, S., Bernard, B. & Stebbins, G. T. The malignant course of ‘benign hallucinations’ in Parkinson disease. Arch. Neurol. 63, 713–716 (2006).
Fénelon, G., Soulas, T., de Langavant, L. C., Trinkler, I. & Bachoud-Lévi, A.-C. Feeling of presence in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 82, 1219–1224 (2011).
Lenka, A., Pagonabarraga, J., Pal, P. K., Bejr-Kasem, H. & Kulisvesky, J. Minor hallucinations in Parkinson disease: a subtle symptom with major clinical implications. Neurology http://doi.org/10.1212/WNL.0000000000007913 (2019).
Ravina, B. et al. Diagnostic criteria for psychosis in Parkinson’s disease: report of an NINDS, NIMH work group. Mov. Disord. 22, 1061–1068 (2007).
Pagonabarraga, J. et al. Neural correlates of minor hallucinations in non-demented patients with Parkinson’s disease. Parkinsonism Relat. Disord. 20, 290–296 (2014).
Bejr-Kasem, H. et al. Minor hallucinations reflect early gray matter loss and predict subjective cognitive decline in Parkinson’s disease. Eur. J. Neurol. 28, 438–447 (2021).
Rosenthal, R. & Fode, K. L. Psychology of the scientist: V. Three experiments in experimenter bias. Psychol. Rep. 12, 491–511 (1963).
Adler, N. E. Impact of prior sets given experimenters and subjects on the experimenter expectancy effect. Sociometry 36, 113–126 (1973).
Rogers, S., Keogh, R. & Pearson, J. Hallucinations on demand: the utility of experimentally induced phenomena in hallucination research. Philos. Trans. R. Soc. B 376, 20200233 (2021).
Blanke, O. et al. Neurological and robot-controlled induction of an apparition. Curr. Biol. 24, 2681–2686 (2014).
Hara, M. et al. A novel manipulation method of human body ownership using an fMRI-compatible master–slave system. J. Neurosci. Methods 235, 25–34 (2014).
Bernasconi, F. et al. Robot-induced hallucinations in Parkinson’s disease depend on altered sensorimotor processing in fronto-temporal network. Sci. Transl. Med. 13, eabc8362 (2021).
Salomon, R. et al. Sensorimotor induction of auditory misattribution in early psychosis. Schizophr. Bull. http://doi.org/10.1093/schbul/sbz136 (2020).
Ford, J. M. & Mathalon, D. H. Electrophysiological evidence of corollary discharge dysfunction in schizophrenia during talking and thinking. J. Psychiatr. Res. 38, 37–46 (2004).
Heinks-Maldonado, T. H. et al. Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations. Arch. Gen. Psychiatry 64, 286–296 (2007).
Brugger, P., Regard, M. & Landis, T. Unilaterally felt ‘presences’: the neuropsychiatry of one’s invisible doppelganger. Cogn. Behav. Neurol. 9, 114–122, (1996).
Blanke, O., Ortigue, S., Coeytaux, A., Martory, M.-D. & Landis, T. Hearing of a presence. Neurocase 9, 329–339 (2003).
Arzy, S., Seeck, M., Ortigue, S., Spinelli, L. & Blanke, O. Induction of an illusory shadow person. Nature 443, 287 (2006).
Blakemore, S. J., Wolpert, D. & Frith, C. Why can’t you tickle yourself? Neuroreport 11, R11–R16 (2000).
Ehrsson, H. H., Holmes, N. P. & Passingham, R. E. Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. J. Neurosci. J. Soc. Neurosci. 25, 10564–10573 (2005).
Ionta, S. et al. Multisensory mechanisms in temporo-parietal cortex support self- and first-person perspective. Neuron 70, 363–374 (2011).
Hara, M. et al. A novel approach to the manipulation of body-parts ownership using a bilateral master-slave system. In 2011 IEEE/RSJ International Conference on Intelligent Robots and Systems 4664–4669 (IEEE, RSJ, 2011); http://doi.org/10.1109/IROS.2011.6094879
Serino, A. et al. Thought consciousness and source monitoring depend on robotically controlled sensorimotor conflicts and illusory states. iScience 24, 101955 (2021).
Weiskrantz, L., Elliott, J. & Darlington, C. Preliminary observations on tickling oneself. Nature 230, 598–599 (1971).
Pozeg, P., Rognini, G., Salomon, R. & Blanke, O. Crossing the hands increases illusory self-touch. PLoS ONE 9, e94008 (2014).
Blanke, O., Slater, M. & Serino, A. Behavioral, neural, and computational principles of bodily self-consciousness. Neuron 88, 145–166 (2015).
Park, H.-D. & Blanke, O. Coupling inner and outer body for self-consciousness. Trends Cogn. Sci. 23, 377–388 (2019).
Kahn, R. S. et al. Schizophrenia. Nat. Rev. Dis. Prim. 1, 1–23 (2015).
Fletcher, P. C. & Frith, C. D. Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nat. Rev. Neurosci. 10, 48–58 (2009).
Orepic, P., Rognini, G., Kannape, O. A., Faivre, N. & Blanke, O. Sensorimotor conflicts induce somatic passivity and louden quiet voices in healthy listeners. Schizophr. Res. 231, 170–177 (2021).
Stripeikyte, G. et al. Fronto-temporal disconnection within the presence hallucination network in psychotic patients with passivity experiences. Schizophr. Bull. 47, 1718–1728 (2021).
Jones, S. A. V. & O’Brien, J. T. The prevalence and incidence of dementia with Lewy bodies: a systematic review of population and clinical studies. Psychol. Med. 44, 673–683 (2014).
Nicolas Nicastro, Stripeikyte, G., Assal, F., Garibotto, V. & Blanke, O. Premotor and fronto-striatal mechanisms associated with presence hallucinations in dementia with Lewy bodies. Neuroimage Clin. (in the press).
Soulas, T., Cleret de Langavant, L., Monod, V. & Fénelon, G. The prevalence and characteristics of hallucinations, delusions and minor phenomena in a non-demented population sample aged 60 years and over. Int. J. Geriatr. Psychiatry 31, 1322–1328 (2016).
O’Callaghan, C. et al. Impaired sensory evidence accumulation and network function in Lewy body dementia. Brain Commun. http://doi.org/10.1093/braincomms/fcab089 (2021).
Schumacher, J. et al. Functional connectivity in mild cognitive impairment with Lewy bodies. J. Neurol. http://doi.org/10.1007/s00415-021-10580-z (2021).
Allefeld, C., Pütz, P., Kastner, K. & Wackermann, J. Flicker-light induced visual phenomena: frequency dependence and specificity of whole percepts and percept features. Conscious. Cogn. 20, 1344–1362 (2011).
Wackermann, J., Pütz, P. & Allefeld, C. Ganzfeld-induced hallucinatory experience, its phenomenology and cerebral electrophysiology. Cortex 44, 1364–1378 (2008).
Mason, O. J. & Brady, F. The psychotomimetic effects of short-term sensory deprivation. J. Nerv. Ment. Dis. 197, 783–785 (2009).
Merabet, L. B. et al. Visual hallucinations during prolonged blindfolding in sighted subjects. J. Neuro-Ophthalmol. 24, 109–113 (2004).
Zarkali, A., Lees, A. J. & Weil, R. S. Flickering stimuli do not reliably induce visual hallucinations in Parkinson’s disease. J. Park. Dis. 9, 631–635 (2019).
Ellson, D. G. Hallucinations produced by sensory conditioning. J. Exp. Psychol. 28, 1–20 (1941).
Powers, A. R., Mathys, C. & Corlett, P. R. Pavlovian conditioning–induced hallucinations result from overweighting of perceptual priors. Science 357, 596–600 (2017).
Vollenweider, F. X. & Preller, K. H. Psychedelic drugs: neurobiology and potential for treatment of psychiatric disorders. Nat. Rev. Neurosci. 21, 611–624 (2020).
Carhart-Harris, R. L. How do psychedelics work? Curr. Opin. Psychiatry 32, 16–21 (2019).
Parvizi, J. et al. Altered sense of self during seizures in the posteromedial cortex. Proc. Natl Acad. Sci. USA 118, e2100522118 (2021).
Penfield, W. & Perot, P. The brain’s record of auditory and visual experience. A final summary and discussion. Brain 86, 595–696 (1963).
Heydrich, L., Lopez, C., Seeck, M. & Blanke, O. Partial and full own-body illusions of epileptic origin in a child with right temporoparietal epilepsy. Epilepsy Behav. 20, 583–586 (2011).
Blanke, O., Perrig, S., Thut, G., Landis, T. & Seeck, M. Simple and complex vestibular responses induced by electrical cortical stimulation of the parietal cortex in humans. J. Neurol. Neurosurg. Psychiatry 69, 553–556 (2000).
Penfield, W. & Boldrey, E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443 (1937).
Frith, C. D. & Done, D. J. Experiences of alien control in schizophrenia reflect a disorder in the central monitoring of action. Psychol. Med. 19, 359–363 (1989).
Tsakiris, M., Hesse, M. D., Boy, C., Haggard, P. & Fink, G. R. Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb. Cortex 17, 2235–2244 (2007).
Ehrsson, H. H., Spence, C. & Passingham, R. E. That’s my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305, 875–877 (2004).
Lenggenhager, B., Tadi, T., Metzinger, T. & Blanke, O. Video ergo sum: manipulating bodily self-consciousness. Science 317, 1096–1099 (2007).
Farrer, C., Valentin, G. & Hupé, J. M. The time windows of the sense of agency. Conscious. Cogn. 22, 1431–1441 (2013).
Blakemore, S.-J., Wolpert, D. M. & Frith, C. D. Central cancellation of self-produced tickle sensation. Nat. Neurosci. 1, 635–640 (1998).
Oldfield, R. C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).
Gorgolewski, K. J. et al. The brain imaging data structure, a format for organizing and describing outputs of neuroimaging experiments. Sci. Data 3, 160044 (2016).
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L. & Petersen, S. E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142–2154 (2012).

Neuroscience robotics for controlled induction and real-time assessment of hallucinations

Supplementary information

Supplementary Information

Reporting Summary

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