Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T17:22:23.096Z Has data issue: false hasContentIssue false

Cortical salience network activation precedes the development of delusion severity

Published online by Cambridge University Press:  18 July 2016

T. T. Raij*
Affiliation:
Department of Psychiatry, Helsinki University and Helsinki University Hospital, Helsinki, Finland Department of Neuroscience and Biomedical Engineering and Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland
T. Mäntylä
Affiliation:
Department of Neuroscience and Biomedical Engineering and Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland Mental Health Unit, National Institute for Health and Welfare, Helsinki, Finland Institute of Behavioral Sciences, University of Helsinki, Helsinki, Finland
O. Mantere
Affiliation:
Department of Psychiatry, Helsinki University and Helsinki University Hospital, Helsinki, Finland
T. Kieseppä
Affiliation:
Department of Psychiatry, Helsinki University and Helsinki University Hospital, Helsinki, Finland Mental Health Unit, National Institute for Health and Welfare, Helsinki, Finland
J. Suvisaari
Affiliation:
Mental Health Unit, National Institute for Health and Welfare, Helsinki, Finland
*
*Address for correspondence: Dr T. T. Raij, Advanced Magnetic Imaging Centre, PO Box 13000, FI-00076 Aalto, Finland. (Email: [email protected])

Abstract

Background

Delusion is the most characteristic symptom of psychosis. While researchers suggested an association between changes of the cortical salience network (CSN) and delusion, whether these CSN findings are a cause or a consequence of delusion remains unknown.

Method

To assess the effect of CSN functioning to forthcoming changes in delusion scores, we measured brain activation with 3-T functional magnetic resonance imaging in two independent samples of first-episode psychosis patients (total of 27 patients and 23 healthy controls). During scanning, the patients evaluated statements about whether an individual's psychosis-related experiences should be described as a mental illness, and control statements that were also evaluated by healthy controls. Symptoms were assessed at the baseline and at 2 months follow-up with Brief Psychiatric Rating Scale.

Results

Both tasks activated the CSN in comparison with rest. Activation of CSN (‘illness evaluation v. control task’ contrast) in patients positively correlated with worsening of or less improvement in delusions at the 2-month follow-up assessment. This finding was independent of delusion and clinical insight scores at the baseline evaluation.

Conclusions

Our findings link symptom-evaluation-related CSN functioning to severity of delusion and, importantly, add a new layer of evidence for the contribution of CSN functioning to the longitudinal course of delusions.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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

Allen, P, Chaddock, CA, Egerton, A, Howes, OD, Barker, G, Bonoldi, I, Fusar-Poli, P, Murray, R, McGuire, P (2015). Functional outcome in people at high risk for psychosis predicted by thalamic glutamate levels and prefronto-striatal activation. Schizophrenia Bulletin 41, 429439.CrossRefGoogle ScholarPubMed
Allen, P, Luigjes, J, Howes, OD, Egerton, A, Hirao, K, Valli, I, Kambeitz, J, Fusar-Poli, P, Broome, M, McGuire, P (2012). Transition to psychosis associated with prefrontal and subcortical dysfunction in ultra high-risk individuals. Schizophrenia Bulletin 38, 12681276.Google Scholar
Allman, JM, Watson, KK, Tetreault, NA, Hakeem, AY (2005). Intuition and autism: a possible role for Von Economo neurons. Trends in Cognitive Sciences 9, 367373.Google Scholar
Andreasen, NC, Pressler, M, Nopoulos, P, Miller, D, Ho, BC (2010). Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biological Psychiatry 67, 255262.Google Scholar
Birchwood, M, Smith, J, Drury, V, Healy, J, Macmillan, F, Slade, M (1994). A self-report Insight Scale for psychosis: reliability, validity and sensitivity to change. Acta Psychiatrica Scandinavica 89, 6267.Google Scholar
Cascella, NG, Gerner, GJ, Fieldstone, SC, Sawa, A, Schretlen, DJ (2011). The insula-claustrum region and delusions in schizophrenia. Schizophrenia Research 133, 7781.Google Scholar
Chao-Gan, Y, Yu-Feng, Z (2010). DPARSF: a MATLAB toolbox for ‘pipeline’ data analysis of resting-state fMRI. Frontiers in Systems Neuroscience 4, 13.Google ScholarPubMed
Chase, HW, Kumar, P, Eickhoff, SB, Dombrovski, AY (2015). Reinforcement learning models and their neural correlates: an activation likelihood estimation meta-analysis. Cognitive, Affective, and Behavioral Neuroscience 15, 435459.Google Scholar
Corlett, PR, Honey, GD, Krystal, JH, Fletcher, PC (2011). Glutamatergic model psychoses: prediction error, learning, and inference. Neuropsychopharmacology 36, 294315.Google Scholar
Craig, AD (2009). How do you feel–now? The anterior insula and human awareness. Nature Reviews Neuroscience 10, 5970.CrossRefGoogle Scholar
Crespo-Facorro, B, Kim, J, Andreasen, NC, O'Leary, DS, Bockholt, HJ, Magnotta, V (2000). Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of first-episode patients. Schizophrenia Research 46, 3543.Google Scholar
Fletcher, PC, Frith, CD (2009). Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nature Reviews Neuroscience 10, 4858.CrossRefGoogle ScholarPubMed
Forsyth, JK, McEwen, SC, Gee, DG, Bearden, CE, Addington, J, Goodyear, B, Cadenhead, KS, Mirzakhanian, H, Cornblatt, BA, Olvet, DM, Mathalon, DH, McGlashan, TH, Perkins, DO, Belger, A, Seidman, LJ, Thermenos, HW, Tsuang, MT, van Erp, TG, Walker, EF, Hamann, S, Woods, SW, Qiu, M, Cannon, TD (2014). Reliability of functional magnetic resonance imaging activation during working memory in a multi-site study: analysis from the North American Prodrome Longitudinal Study. Neuroimage 97, 4152.Google Scholar
Gee, DG, McEwen, SC, Forsyth, JK, Haut, KM, Bearden, CE, Addington, J, Goodyear, B, Cadenhead, KS, Mirzakhanian, H, Cornblatt, BA, Olvet, D, Mathalon, DH, McGlashan, TH, Perkins, DO, Belger, A, Seidman, LJ, Thermenos, H, Tsuang, MT, van Erp, TG, Walker, EF, Hamann, S, Woods, SW, Constable, T, Cannon, TD (2015). Reliability of an fMRI paradigm for emotional processing in a multisite longitudinal study. Human Brain Mapping 36, 25582579.Google Scholar
Gilleen, J, David, AS (2005). The cognitive neuropsychiatry of delusions: from psychopathology to neuropsychology and back again. Psychological Medicine 35, 512.Google Scholar
Gradin, VB, Kumar, P, Waiter, G, Ahearn, T, Stickle, C, Milders, M, Reid, I, Hall, J, Steele, JD (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain 134, 17511764.Google Scholar
Grant, AM (2002). The self-reflection and insight scale: a new measure of private self-consciousness. Social Behavior and Personality 30, 821836.CrossRefGoogle Scholar
Henriksen, MG, Parnas, J (2014). Self-disorders and schizophrenia: a phenomenological reappraisal of poor insight and noncompliance. Schizophrenia Bulletin 40, 542547.Google Scholar
Howes, OD, Kambeitz, J, Kim, E, Stahl, D, Slifstein, M, Abi-Dargham, A, Kapur, S (2012). The nature of dopamine dysfunction in schizophrenia and what this means for treatment. Archives of General Psychiatry 69, 776786.Google Scholar
Hu, C, Di, X, Eickhoff, SB, Zhang, M, Peng, K, Guo, H, Sui, J (2016). Distinct and common aspects of physical and psychological self-representation in the brain: a meta-analysis of self-bias in facial and self-referential judgements. Neuroscience and Biobehavioral Reviews 61, 197-207.Google Scholar
Jardri, R, Pouchet, A, Pins, D, Thomas, P (2011). Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Americam Journal of Psychiatry 168, 7381.Google 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.Google Scholar
Koutsouleris, N, Gaser, C, Jager, M, Bottlender, R, Frodl, T, Holzinger, S, Schmitt, GJ, Zetzsche, T, Burgermeister, B, Scheuerecker, J, Born, C, Reiser, M, Moller, HJ, Meisenzahl, EM (2008). Structural correlates of psychopathological symptom dimensions in schizophrenia: a voxel-based morphometric study. Neuroimage 39, 16001612.Google Scholar
Kriegeskorte, N, Simmons, WK, Bellgowan, PSF (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience 12, 535540.Google Scholar
Manoliu, A, Riedl, V, Zherdin, A, Muhlau, M, Schwerthoffer, D, Scherr, M, Peters, H, Zimmer, C, Forstl, H, Bauml, J, Wohlschlager, AM, Sorg, C (2014). Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. Schizophrenia Bulletin 40, 428437.Google Scholar
Mäntylä, T, Mantere, O, Raij, TT, Kieseppä, T, Laitinen, H, Leiviskä, J, Torniainen, M, Tuominen, L, Vaarala, O, Suvisaari, J (2015). Altered activation of innate immunity associates with white matter volume and diffusion in first-episode psychosis. PLoS ONE 10, e0125112.Google Scholar
McEvoy, JP, Apperson, LJ, Appelbaum, PS, Ortlip, P, Brecosky, J, Hammill, K, Geller, JL, Roth, L (1989). Insight in schizophrenia. Its relationship to acute psychopathology. Journal of Nervous and Mental Disease 177, 4347.Google Scholar
Menon, M, Schmitz, TW, Anderson, AK, Graff, A, Korostil, M, Mamo, D, Gerretsen, P, Addington, J, Remington, G, Kapur, S (2011). Exploring the neural correlates of delusions of reference. Biological Psychiatry 70, 11271133.Google Scholar
Menon, V, Uddin, LQ (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 214, 655667.Google Scholar
Modinos, G, Ormel, J, Aleman, A (2009). Activation of anterior insula during self-reflection. PLoS ONE 4, e4618.Google Scholar
Murray, GK, Corlett, PR, Clark, L, Pessiglione, M, Blackwell, AD, Honey, G, Jones, PB, Bullmore, ET, Robbins, TW, Fletcher, PC (2008). Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Molecular Psychiatry 13, 239, 267276.Google Scholar
Orliac, F, Naveau, M, Joliot, M, Delcroix, N, Razafimandimby, A, Brazo, P, Dollfus, S, Delamillieure, P (2013). Links among resting-state default-mode network, salience network, and symptomatology in schizophrenia. Schizophrenia Research 148, 7480.Google Scholar
Palaniyappan, L, Liddle, PF (2012). Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. Journal of Psychiatry and Neuroscience 37, 1727.Google Scholar
Palaniyappan, L, Mallikarjun, P, Joseph, V, White, TP, Liddle, PF (2011). Reality distortion is related to the structure of the salience network in schizophrenia. Psychological Medicine 41, 17011708.Google Scholar
Palaniyappan, L, Simmonite, M, White, TP, Liddle, EB, Liddle, PF (2013). Neural primacy of the salience processing system in schizophrenia. Neuron 79, 814828.Google Scholar
Radaelli, D, Poletti, S, Gorni, I, Locatelli, C, Smeraldi, E, Colombo, C, Benedetti, F (2014). Neural correlates of delusion in bipolar depression. Psychiatry Research 221, 15.Google Scholar
Raij, TT, Mäntylä, T, Kieseppä, T, Suvisaari, J (2015). Aberrant functioning of the putamen links delusions, antipsychotic drug dose, and compromised connectivity in first episode psychosis-Preliminary fMRI findings. Psychiatry Research 233, 201211.CrossRefGoogle ScholarPubMed
Sabb, FW, van Erp, TG, Hardt, ME, Dapretto, M, Caplan, R, Cannon, TD, Bearden, CE (2010). Language network dysfunction as a predictor of outcome in youth at clinical high risk for psychosis. Schizophrenia Research 116, 173183.Google Scholar
Samanez-Larkin, GR, Hollon, NG, Carstensen, LL, Knutson, B (2008). Individual differences in insular sensitivity during loss anticipation predict avoidance learning. Psychological Science 19, 320323.Google Scholar
Shirer, WR, Ryali, S, Rykhlevskaia, E, Menon, V, Greicius, MD (2012). Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebral Cortex 22, 158165.Google Scholar
van der Gaag, M (2006). A neuropsychiatric model of biological and psychological processes in the remission of delusions and auditory hallucinations. Schizophrenia Bulletin 32 (Suppl. 1), S113S122.Google Scholar
van Veen, V, Krug, MK, Schooler, JW, Carter, CS (2009). Neural activity predicts attitude change in cognitive dissonance. Nature Neuroscience 12, 14691474.Google Scholar
Ventura, J, Lukoff, D, Nuechterlein, KH, Liberman, RP, Green, MF, Shaner, A (1993). Brief psychiatric rating scale (BPRS) expanded version: scales, anchor points, and administration manual. International Journal of Methods in Psychiatric Research 3, 227243.Google Scholar
Wells, A, Cartwright-Hatton, S (2004). A short form of the metacognitions questionnaire: properties of the MCQ-30. Behaviour Research and Therapy 42, 385396.Google Scholar
Woo, CW, Krishnan, A, Wager, TD (2014). Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 91, 412419.Google Scholar
Supplementary material: File

Raij supplementary material

Raij supplementary material

Download Raij supplementary material(File)
File 368.1 KB