Self-other recognition impairments in individuals with schizophrenia: a new experimental paradigm using a double mirror

Gaelle Keromnes, Tom Motillon, Nathalie Coulon, Alain Berthoz, Foucaud Du Boisgueheneuc, Moritz Wehrmann, Brice Martin, Bérangère Thirioux, Olivier Bonnot, Romain Ridereau, Eric Bellissant, Dominique Drapier, David Levoyer, Nemat Jaafari, Sylvie Tordjman, Gaelle Keromnes, Tom Motillon, Nathalie Coulon, Alain Berthoz, Foucaud Du Boisgueheneuc, Moritz Wehrmann, Brice Martin, Bérangère Thirioux, Olivier Bonnot, Romain Ridereau, Eric Bellissant, Dominique Drapier, David Levoyer, Nemat Jaafari, Sylvie Tordjman

Abstract

Clinical observations suggest early self-consciousness disturbances in schizophrenia. A double mirror combining the images of two individuals sitting on each side of the mirror was used to study self-other differentiation in 12 individuals with early onset schizophrenia (EOS) and 15 individuals with adult onset schizophrenia (AOS) compared to 27 typically developing controls (TDC) matched on age and sex. The effects of intermodal sensory perception (visual-tactile and visual-kinesthetic) on self-other recognition were also studied. The results showed that EOS and AOS individuals, independently of age and schizophrenia severity, were centered on their own image compared to TDC, with both significant earlier self-recognition and delayed other-recognition during the visual recognition task. In addition, there was no significant effect of intermodal sensory stimulation on self-other recognition in EOS and AOS patients, whereas self-centered functioning was significantly increased by visual-tactile stimulation and decreased by visual-kinesthetic stimulation in TDC. The findings suggest that self-other recognition impairments might be a possible endophenotypic trait of schizophrenia.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Distribution plots of M1 and M2 levels in the visual—alone reference condition for individuals with schizophrenia (EOS, AOS, and EOS+AOS) and typically developing controls. a M1 levels and b M2 levels are indicated by squares. Pale squares indicate more than one individual with the same value, whereas dark squares indicate only one individual with the value. EOS individuals with early onset schizophrenia, AOS individuals with adult onset schizophrenia, TDC1 typically developing controls matched with EOS individuals, TDC2 typically developing controls matched with AOS individuals, SCH total group of individuals with schizophrenia (EOS+AOS), TDC total group of typically developing controls (TDC1+TDC2)
Fig. 2
Fig. 2
The experimental setting of the double mirror. a The experiment took place in an entirely darkened enclosed area that was set up inside the testing room in the Research Center of Hospital Guillaume Regnier in Rennes. The mirror was set up on top of a rectangular table. The patient with schizophrenia and his/her matched control were sitting facing each other on both side of the double mirror. b Both participants were wearing a black long-sleeved shirt, a black turtle neck, and black gloves to lessen any possible parasite visual stimulation. They were asked to look straight into each other's eyes and to focus only on the face of the other person. Adjustable chairs allowed to align the participants' eyes. No participants had eyeglasses that would have been objects interfering with the recognition task
Fig. 3
Fig. 3
Simultaneous variations of light intensity on each side of the mirror over the time span of the procedure. At the beginning of the task, the light intensity is at 100% for the TDC individual (corresponding to a total/complete mirror effect), whereas the light intensity is at 0% for the patient (corresponding to a total/complete transparent window). Then the light intensity is progressively increased by 10% steps for the patient to reach 100% on both sides (the light intensity remains at 100% for the TDC individual). In other words, the patient's image appears progressively and is combined more and more with the TDC's image. At this point, the light intensity is progressively decreased by 10% steps for the TDC, whereas the light intensity remains at 100% for the patient (mirror effect). In other words, the TDC image fades away progressively up to its total disappearance when the light intensity drops down to 0%. The reverse procedure is then used to go back to the initial configuration (100% of light intensity corresponding to a total mirror effect for the TDC individual and 0% of light intensity corresponding to a completely transparent window for the patient). Therefore, each stimulus of identical light intensity is presented twice to the participants during one passage back and forth

References

    1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th edn. Arlington, VA: American Psychiatric Publishing; 2013.
    1. Organization WH. ICD-10: The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. Geneva: World Health Organisation; 1992.
    1. Nordgaard J, Revsbech R, Sæbye D, Parnas J. Assessing the diagnostic validity of a structured psychiatric interview in a first-admission hospital sample. World Psychiatry. 2012;11:181–185. doi: 10.1002/j.2051-5545.2012.tb00128.x.
    1. Jansson L, Handest P, Nielsen J, Sæbye D, Parnas J. Exploring boundaries of schizophrenia: a comparison of ICD-10 with other diagnostic systems in first-admitted patients. World Psychiatry. 2002;1:109–114.
    1. Parnas J, Handest P. Phenomenology of anomalous self-experience in early schizophrenia. Compr. Psychiatry. 2003;44:121–134. doi: 10.1053/comp.2003.50017.
    1. Bleuler, E. Dementia Praecox ou Groupe des Schizophrénies (Epel Editions, Paris, 1993) (1st publication 1911).
    1. Kraepelin, E. Leçons Cliniques sur la Démence Précoce et la Psychose Maniaco-Dépressive (Privat, Toulouse, 1970) (1st publication 1899).
    1. Minkowski, E. La Schizophrénie (Payot, Paris, 2002) (1st publication 1927).
    1. Tatossian, A. La phénoménologie des Psychoses. Rapport de Psychiatrie. Angers CPNLF 1979 (Cercle Herméneutique, Paris, 2002).
    1. Parnas J, Henriksen MG. Disordered self in the schizophrenia spectrum: a clinical and research perspective. Harv. Rev. Psychiatry. 2014;22:251–265. doi: 10.1097/HRP.0000000000000040.
    1. Graham KT, Martin-Iverson MT, Holmes NP, Jablensky A, Waters F. Deficits in agency in schizophrenia, and additional deficits in body image, body schema, and internal timing, in passivity symptoms. Front. Psychiatry. 2014;5:126. doi: 10.3389/fpsyt.2014.00126.
    1. Sass LA, Parnas J. Schizophrenia, consciousness, and the self. Schizophr. Bull. 2003;29:427–444. doi: 10.1093/oxfordjournals.schbul.a007017.
    1. Moe AM, Docherty NM. Schizophrenia and the sense of self. Schizophr. Bull. 2014;40:161–168. doi: 10.1093/schbul/sbt121.
    1. Daprati E, et al. Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition. 1997;65:71–86. doi: 10.1016/S0010-0277(97)00039-5.
    1. Remschmidt HE, Theisen F. Early-onset schizophrenia. Neuropsychobiology. 2012;66:63–69. doi: 10.1159/000338548.
    1. McClellan, J., Stock, S. & American Academy of Child and Adolescent Psychiatry (AACAP) Committee on Quality Issues (CQI). Practice parameter for the assessment and treatment of children and adolescents with schizophrenia. J. Am. Acad. Child Adolesc. Psychiatry52, 976–990 (2013).
    1. Zaytseva Y, Korsakova N, Agius M, Gurovich I. Neurocognitive functioning in schizophrenia and during the early phases of psychosis: targeting cognitive remediation interventions. Biomed. Res. Int. 2013;2013:819587. doi: 10.1155/2013/819587.
    1. Schilder P. L’image du Corps. Paris: Gallimard; 1968.
    1. Neisser U. Two perceptually given aspects of the self and their development. Dev. Rev. 1991;11:197–209. doi: 10.1016/0273-2297(91)90009-D.
    1. Wallon H. Le rôle de l’autre dans la conscience du moi. Enfance. 1959;12:277–286. doi: 10.3406/enfan.1959.1443.
    1. Wallon, H. Les Origines du Caractère Chez L’enfant (PUF, Paris, 2002) (1st publication 1934)
    1. Zazzo R. Images du corps et conscience de soi. Enfance. 1948;1:29–43. doi: 10.3406/enfan.1948.1295.
    1. Damasio, A. R., Tiercelin, C. & Larsonneur, C. Le Sentiment Même de soi: Corps, Émotion, Conscience (ed Editions Odile Jacob, Paris, 1999).
    1. Rochat P. Five levels of self-awareness as they unfold early in life. Conscious Cogn. 2003;12:717–731. doi: 10.1016/S1053-8100(03)00081-3.
    1. Decety J, Sommerville JA. Shared representations between self and other: a social cognitive neuroscience view. Trends Cogn. Sci. 2003;7:527–533. doi: 10.1016/j.tics.2003.10.004.
    1. Pasqualini I, Llobera J, Blanke O. ‘Seeing’ and ‘feeling’ architecture: how bodily self-consciousness alters architectonic experience and affects the perception of interiors. Front. Psychol. 2013;4:354. doi: 10.3389/fpsyg.2013.00354.
    1. Ionta S, Gassert R, Blanke O. Multi-sensory and sensorimotor foundation of bodily self-consciousness - an interdisciplinary approach. Front. Psychol. 2011;2:383. doi: 10.3389/fpsyg.2011.00383.
    1. Aspell JE, Lenggenhager B, Blanke O. Keeping in touch with one’s self: multisensory mechanisms of self-consciousness. PLoS ONE. 2009;4:e6488. doi: 10.1371/journal.pone.0006488.
    1. Blanke O. I and me: self-portraiture in brain damage. Front. Neurol. Neurosci. 2007;22:14–29. doi: 10.1159/000102822.
    1. Martin B, et al. Temporal structure of consciousness and minimal self in schizophrenia. Front. Psychol. 2014;5:1175.
    1. Mishara AL, Lysaker PH, Schwartz MA. Self-disturbances in schizophrenia: history, phenomenology, and relevant findings from research on metacognition. Schizophr. Bull. 2014;40:5–12. doi: 10.1093/schbul/sbt169.
    1. Tordjman S, Maillhes AS. Les troubles du développement de l’image du corps dans la petite enfance: une dimension commune partagée dans la schizophrénie et l’autisme? Neuropsychiatr. l’Enfance l’Adolescence. 1954;57:333–340.
    1. Shentoub SA, Soulairac A, Rustin E. Comportement de l’enfant arriéré devant le miroir. Enfance. 1954;7:333–340. doi: 10.3406/enfan.1954.1469.
    1. Delmas FA. Le signe du miroir dans la démence précoce. Ann. Med. Psychol. 1929;1:227–233.
    1. Abely P. Le signe du miroir dans les psychoses et plus spécialement dans la démence précoce. Ann. Med. Psychol. 1930;1:28–36.
    1. Thirioux B, Wehrmann M, Langbour N, Jaafari N, Berthoz A. Identifying oneself with the face of someone else impairs the egocentered visuo-spatial mechanisms: a new double mirror paradigm to study self-other distinction and interaction. Front. Psychol. 2016;7:1283.
    1. Hur JW, Kwon JS, Lee TY, Park S. The crisis of minimal self-awareness in schizophrenia: a meta-analytic review. Schizophr. Res. 2014;152:58–64. doi: 10.1016/j.schres.2013.08.042.
    1. Gallagher S, Trigg D. Agency and anxiety: delusions of control and loss of control in schizophrenia and agoraphobia. Front. Hum. Neurosci. 2016;10:459. doi: 10.3389/fnhum.2016.00459.
    1. McTeague LM, et al. Identification of common neural circuit disruptions in cognitive control across psychiatric disorders. AJP. 2017;174:676–685. doi: 10.1176/appi.ajp.2017.16040400.
    1. Pankow A, et al. Aberrant salience is related to dysfunctional self-referential processing in psychosis. Schizophr. Bull. 2016;42:67–76.
    1. Zhou Y, et al. Altered intrinsic and extrinsic connectivity in schizophrenia. Neuroimage Clin. 2018;17:704–716. doi: 10.1016/j.nicl.2017.12.006.
    1. Sulpizio V, et al. Visuospatial transformations and personality: evidence of a relationship between visuospatial perspective taking and self-reported emotional empathy. Exp. Brain Res. 2015;233:2091–2102. doi: 10.1007/s00221-015-4280-2.
    1. Thirioux B, Tandonnet L, Jaafari N, Berthoz A. Disturbances of spontaneous empathic processing relate with the severity of the negative symptoms in patients with schizophrenia: a behavioural pilot-study using virtual reality technology. Brain Cogn. 2014;90:87–99. doi: 10.1016/j.bandc.2014.06.006.
    1. Thakkar KN, Nichols HS, McIntosh LG, Park S. Disturbances in body ownership in schizophrenia: evidence from the rubber hand illusion and case study of a spontaneous out-of-body experience. PLoS ONE. 2011;6:e27089. doi: 10.1371/journal.pone.0027089.
    1. Williams LE, Light GA, Braff DL, Ramachandran VS. Reduced multisensory integration in patients with schizophrenia on a target detection task. Neuropsychologia. 2010;48:3128–3136. doi: 10.1016/j.neuropsychologia.2010.06.028.
    1. Tseng HH, et al. A systematic review of multisensory cognitive-affective integration in schizophrenia. Neurosci. Biobehav. Rev. 2015;55:444–452. doi: 10.1016/j.neubiorev.2015.04.019.
    1. Wallace MT, Stevenson RA. The construct of the multisensory temporal binding window and its dysregulation in developmental disabilities. Neuropsychologia. 2014;64:105–123. doi: 10.1016/j.neuropsychologia.2014.08.005.
    1. Peters SK, Dunlop K, Downar J. Cortico-striatal-thalamic loop circuits of the salience network: a central pathway in psychiatric disease and treatment. Front. Syst. Neurosci. 2016;10:104. doi: 10.3389/fnsys.2016.00104.
    1. Abramov I, et al. The retina of the newborn human infant. Science. 1982;217:265–267. doi: 10.1126/science.6178160.
    1. Issel EP. Fetal response to external mechanical stimulation. J. Perinat. Med. 1983;11:232–242. doi: 10.1515/jpme.1983.11.5.232.
    1. Howes OD, Murray RM. Schizophrenia: an integrated sociodevelopmental-cognitive model. Lancet. 2014;383:1677–1687. doi: 10.1016/S0140-6736(13)62036-X.

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