Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-27T03:52:14.329Z Has data issue: false hasContentIssue false

Neural correlates of referential/persecutory delusions in schizophrenia: examination using fMRI and a virtual reality underground travel paradigm

Published online by Cambridge University Press:  22 June 2022

Paola Fuentes-Claramonte
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Pilar Salgado-Pineda
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Isabel Argila-Plaza
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain
María Ángeles García-León
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Núria Ramiro
Affiliation:
Psychiatry Department, Hospital Sant Rafael, Barcelona, Spain
Joan Soler-Vidal
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain Benito Menni Centre Assistencial en Salut Mental, Sant Boi de Llobregat, Barcelona, Spain
Auria Albacete
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Nicolas Delgado
Affiliation:
Qmenta, Barcelona, Spain
Paulo Tavares
Affiliation:
Qmenta, Barcelona, Spain
María Llanos Torres
Affiliation:
Hospital Mare de Dèu de la Mercé, Unitat Polivalent, Barcelona, Spain
Amalia Guerrero-Pedraza
Affiliation:
Benito Menni Centre Assistencial en Salut Mental, Sant Boi de Llobregat, Barcelona, Spain
Francisco Portillo
Affiliation:
Benito Menni Centre Assistencial en Salut Mental, Sant Boi de Llobregat, Barcelona, Spain
Ester Boix
Affiliation:
Mental Health Department, Hospital de Mataró, Mataró, Spain
Josep Munuera
Affiliation:
Diagnostic Imaging Department, Hospital Sant Joan de Déu, Barcelona, Spain
Antonio Arévalo
Affiliation:
Hospital Sagrat Cor, Martorell, Barcelona, Spain
Salvador Sarró
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Raymond Salvador
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Peter J. McKenna*
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
Edith Pomarol-Clotet
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM (Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain
*
Author for correspondence: Peter J. McKenna, E-mail: mckennapeter1@gmail.com

Abstract

Background

The brain functional correlates of delusions have been relatively little studied. However, a virtual reality paradigm simulating travel on the London Underground has been found to evoke referential ideation in both healthy subjects and patients with schizophrenia, making brain activations in response to such experiences potentially identifiable.

Method

Ninety patients with schizophrenia/schizoaffective disorder and 28 healthy controls underwent functional magnetic resonance imaging while they viewed virtual reality versions of full and empty Barcelona Metro carriages.

Results

Compared to the empty condition, viewing the full carriage was associated with activations in the visual cortex, the cuneus and precuneus/posterior cingulate cortex, the inferior parietal cortex, the angular gyrus and parts of the middle and superior temporal cortex including the temporoparietal junction bilaterally. There were no significant differences in activation between groups. Nor were there activations associated with referentiality or presence of delusions generally in the patient group. However, patients with persecutory delusions showed a cluster of reduced activation compared to those without delusions in a region in the right temporal/occipital cortex.

Conclusions

Performance of the metro task is associated with a widespread pattern of activations, which does not distinguish schizophrenic patients and controls, or show an association with referentiality or delusions in general. However, the finding of a cluster of reduced activation close to the right temporoparietal junction in patients with persecutory delusions specifically is of potential interest, as this region is believed to play a role in social cognition.

Type
Original Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in fMRI. Neuroimage, 20, 10521063.CrossRefGoogle Scholar
Bleuler, E. (1911). Dementia praecox or the group of schizophrenias (translated by J. Zinkin, 1950). New York: International Universities Press.Google Scholar
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 138.CrossRefGoogle ScholarPubMed
Buckner, R. L., & DiNicola, L. M. (2019). The brain's default network: Updated anatomy, physiology and evolving insights. Nature Reviews: Neuroscience, 20, 593608.CrossRefGoogle ScholarPubMed
Das, P., Lagopoulos, J., Coulston, C. M., Henderson, A. F., & Malhi, G. S. (2012). Mentalizing impairment in schizophrenia: A functional MRI study. Schizophrenia Research, 134, 158164.CrossRefGoogle ScholarPubMed
Decety, J., & Lamm, C. (2007). The role of the right temporoparietal junction in social interaction: How low-level computational processes contribute to meta-cognition. Neuroscientist, 13, 580593.CrossRefGoogle ScholarPubMed
Del Ser, T., Gonzalez-Montalvo, J. I., Martinez-Espinosa, S., Delgado-Villapalos, C., & Bermejo, F. (1997). Estimation of premorbid intelligence in Spanish people with the word accentuation test and its application to the diagnosis of dementia. Brain and Cognition, 33, 343356.CrossRefGoogle Scholar
Eddy, C. M. (2016). The junction between self and other? Temporo-parietal dysfunction in neuropsychiatry. Neuropsychologia, 89, 465477.CrossRefGoogle ScholarPubMed
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the USA, 113, 79007905.CrossRefGoogle ScholarPubMed
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). The structured clinical interview for DSM-IV axis I disorders (research version). New York: Biometrics Research, New York State Psychiatric Institute.Google Scholar
Freeman, D. (2007). Suspicious minds: The psychology of persecutory delusions. Clinical Psychology Review, 27, 425457.CrossRefGoogle ScholarPubMed
Freeman, D., Pugh, K., Antley, A., Slater, M., Bebbington, P., Gittins, M., … Garety, P. (2008). Virtual reality study of paranoid thinking in the general population. British Journal of Psychiatry, 192, 258263.CrossRefGoogle ScholarPubMed
Freeman, D., Pugh, K., Green, C., Valmaggia, L., Dunn, G., & Garety, P. (2007). A measure of state persecutory ideation for experimental studies. Journal of Nervous and Mental Disease, 195, 781784.CrossRefGoogle ScholarPubMed
Freeman, D., Pugh, K., Vorontsova, N., Antley, A., & Slater, M. (2010). Testing the continuum of delusional beliefs: An experimental study using virtual reality. Journal of Abnormal Psychology, 119, 8392.CrossRefGoogle ScholarPubMed
Frith, C. D. (1992). The cognitive neuropsychology of schizophrenia. Hove: Erlbaum, UK: Taylor & Francis.Google Scholar
Frith, C. D. (2004). Schizophrenia and theory of mind. Psychological Medicine, 34, 385389.CrossRefGoogle ScholarPubMed
Fuentes-Claramonte, P., Martin-Subero, M., Salgado-Pineda, P., Santo-Angles, A., Argila-Plaza, I., Salavert, J., … Salvador, R. (2020). Brain imaging correlates of self- and other-reflection in schizophrenia. Neuroimage: Clinical, 25, 102134.CrossRefGoogle ScholarPubMed
Gomar, J. J., Ortiz-Gil, J., McKenna, P. J., Salvador, R., Sans-Sansa, B., Sarro, S., … Pomarol-Clotet, E. (2011). Validation of the word accentuation test (TAP) as a means of estimating premorbid IQ in Spanish speakers. Schizophrenia Research, 128, 175176.CrossRefGoogle ScholarPubMed
Haddock, G., McCarron, J., Tarrier, N., & Faragher, E. B. (1999). Scales to measure dimensions of hallucinations and delusions: The psychotic symptom rating scales (PSYRATS). Psychological Medicine, 29, 879889.CrossRefGoogle ScholarPubMed
Hollerman, J. R., Tremblay, L., & Schultz, W. (2000). Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. Progress in Brain Research, 126, 193215.CrossRefGoogle ScholarPubMed
Jauhar, S., Fortea, L., Solanes, A., Albajes-Eizagirre, A., McKenna, P. J., & Radua, J. (2021). Brain activations associated with anticipation and delivery of monetary reward: A systematic review and meta-analysis of fMRI studies. PLoS ONE, 16, e0255292.CrossRefGoogle Scholar
Kapur, S. (2003). Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry, 160, 1323.CrossRefGoogle ScholarPubMed
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261276.CrossRefGoogle ScholarPubMed
Kraepelin, E. (1913). Dementia praecox and paraphrenia (translated by R.M. Barclay, 1919). Edinburgh: Livingstone.Google Scholar
Kronbichler, L., Tschernegg, M., Martin, A. I., Schurz, M., & Kronbichler, M. (2017). Abnormal brain activation during theory of mind tasks in schizophrenia: A meta-analysis. Schizophrenia Bulletin, 43, 12401250.CrossRefGoogle ScholarPubMed
McKenna, P. (2017). Delusions: Understanding the un-understandable. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Menon, M., Schmitz, T. W., Anderson, A. K., Graff, A., Korostil, M., Mamo, D., … Kapur, S. (2011). Exploring the neural correlates of delusions of reference. Biological Psychiatry, 70, 11271133.CrossRefGoogle ScholarPubMed
Molenberghs, P., Johnson, H., Henry, J. D., & Mattingley, J. B. (2016). Understanding the minds of others: A neuroimaging meta-analysis. Neuroscience and Biobehavioral Reviews, 65, 276291.CrossRefGoogle ScholarPubMed
Nelson, H. E., & Willison, J. R. (1991). The revised national adult reading test. Windsor, Berks: NFER-Nelson.Google Scholar
Oldham, S., Murawski, C., Fornito, A., Youssef, G., Yucel, M., & Lorenzetti, V. (2018). The anticipation and outcome phases of reward and loss processing: A neuroimaging meta-analysis of the monetary incentive delay task. Human Brain Mapping, 39, 33983418.CrossRefGoogle ScholarPubMed
Radua, J., Schmidt, A., Borgwardt, S., Heinz, A., Schlagenhauf, F., McGuire, P., & Fusar-Poli, P. (2015). Ventral striatal activation during reward processing in psychosis: A neurofunctional meta-analysis. JAMA Psychiatry, 72, 12431251.CrossRefGoogle ScholarPubMed
Salgado-Pineda, P., Fuentes-Claramonte, P., Spanlang, B., Pomes, A., Landin-Romero, R., Portillo, F., … Pomarol-Clotet, E. (2022). Neural correlates of disturbance in the sense of agency in schizophrenia: An fMRI study using the ‘enfacement’ paradigm. Schizophrenia Research, 243, 395–401.CrossRefGoogle ScholarPubMed
Schultz, W., Tremblay, L., & Hollerman, J. R. (2000). Reward processing in primate orbitofrontal cortex and basal ganglia. Cerebral Cortex, 10, 272284.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23 (Suppl 1), S208S219.CrossRefGoogle ScholarPubMed
Spreng, R. N., Mar, R. A., & Kim, A. S. (2009). The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: A quantitative meta-analysis. Journal of Cognitive Neuroscience, 21, 489510.CrossRefGoogle Scholar
Vucurovic, K., Caillies, S., & Kaladjian, A. (2020). Neural correlates of theory of mind and empathy in schizophrenia: An activation likelihood estimation meta-analysis. Journal of Psychiatric Research, 120, 163174.CrossRefGoogle ScholarPubMed
Wilkinson, G. S., & Robertson, G. J. (2017). Wide range achievement test professional manual (5th ed.). Bloomington, MN: NCS Pearson, Inc.Google Scholar
Wong, G. H., Hui, C. L., Tang, J. Y., Chiu, C. P., Lam, M. M., Chan, S. K., … Chen, E. Y. (2012). Screening and assessing ideas and delusions of reference using a semi-structured interview scale: A validation study of the ideas of reference interview scale (IRIS) in early psychosis patients. Schizophrenia Research, 135, 158163.CrossRefGoogle Scholar
Supplementary material: File

Fuentes-Claramonte et al. supplementary material

Fuentes-Claramonte et al. supplementary material

Download Fuentes-Claramonte et al. supplementary material(File)
File 49.4 KB