Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T07:16:15.258Z Has data issue: false hasContentIssue false

Mapping prodromal psychosis: A critical review of neuroimaging studies

Published online by Cambridge University Press:  15 April 2020

P. Fusar-Poli*
Affiliation:
Institute of Psychiatry, Department of Psychosis Studies, London, United Kingdom
P. McGuire
Affiliation:
Institute of Psychiatry, Department of Psychosis Studies, London, United Kingdom
S. Borgwardt
Affiliation:
Institute of Psychiatry, Department of Psychosis Studies, London, United Kingdom
*
*Corresponding author. De Crespigny Park 16, Institute of Psychiatry, Department of Psychosis Studies, SE58AF London, United Kingdom. Tel.: +44 7786 666 570; fax: +44 2078 480 976. p.fusar@libero.it (P. Fusar-Poli).
Get access

Abstract

The onset of schizophrenia is usually preceded by a prodromal phase characterized by functional decline and subtle prodromal symptoms, which include attenuated psychotic phenomena, cognitive deterioration and a decline in socio-occupational function. Preventive interventions during this phase are of great interest because of the impressive clinical benefits. However, available psychopathological criteria employed to define a high risk state for psychosis have low validity and specificity. Consequently there is an urgent need of reliable neurocognitive markers linked to the pathophysiological mechanisms that underlie schizophrenia. Neuroimaging techniques have rapidly developed into a powerful tool in psychiatry as they provide an unprecedented opportunity for the investigation of brain structure and function. This review shows that neuroimaging studies of the prodromal phases of psychosis have the potentials to identify core structural and functional markers of an impending risk to psychosis and to clarify the dynamic changes underlying transition to psychosis and to address significant correlations between brain structure or function and prodromal psychopathology. Additionally, neurochemical methods can address the key role played by neurotransmitters such as dopamine and glutamate during the psychosis onset. To conclude, multimodal neuroimaging may ultimately clarify the neurobiology of the prodromal phases by the integration of functional, structural and neurochemical findings.

Type
Reviews
Copyright
Copyright © Elsevier Masson SAS 2012

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., Seal, M.L., Valli, I., Fusar-Poli, P., Perlini, C., Day, F.et al.Altered Prefrontal and Hippocampal Function During Verbal Encoding and Recognition in People With Prodromal Symptoms of Psychosis. Schizophr Bull. 37 4: 2011 746756.CrossRefGoogle ScholarPubMed
Anis, N.A., Berry, S.C., Burton, N.R., Lodge, D.The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methyl-aspartate. Br J Pharmacol. 1983; 79: 565575.CrossRefGoogle ScholarPubMed
Bilder, R.M., Reiter, G., Bates, J., Lencz, T., Szeszko, P., Goldman, R.S.et al.Cognitive development in schizophrenia: follow-back from the first episode. J Clin Exp Neuropsychol. 2006; 28: 270282.CrossRefGoogle ScholarPubMed
Borgwardt, S.J., McGuire, P.K., Aston, J., Berger, G., Dazzan, P., Gschwandtner, U.et al.Structural brain abnormalities in individuals with an at-risk mental state who later develop psychosis. Br J Psychiatry Suppl. 2007; 51: s69s75.CrossRefGoogle ScholarPubMed
Borgwardt, S.J., Riecher-Rossler, A., Dazzan, P., Chitnis, X., Aston, J., Drewe, M.et al.Regional gray matter volume abnormalities in the at-risk mental state. Biol Psychiatry. 2007; 61: 11481156.CrossRefGoogle ScholarPubMed
Borgwardt, S.J., McGuire, P.K., Aston, J., Gschwandtner, U., Pfluger, M.O., Stieglitz, R.D.et al.Reductions in frontal, temporal and parietal volume associated with the onset of psychosis. Schizophr Res. 2008; 106: 108114.CrossRefGoogle Scholar
Borgwardt, S.J., Picchioni, M.M., Ettinger, U., Toulopoulou, T., Murray, R., McGuire, P.K.Regional gray matter volume in monozygotic twins concordant and discordant for schizophrenia. Biol. Psychiatry. 2010; 67: 956964.CrossRefGoogle Scholar
Broome, M.R., Matthiasson, P., Fusar-Poli, P., Woolley, J., Johns, L., Tabraham, P.et al.Neural correlates of executive function and working memory in the “at-risk mental state”. Br J Psychiatry. 2009; 194: 2533.CrossRefGoogle ScholarPubMed
Cahn, W., Hulshoff Pol, H.E., Lems, E.B., van Haren, N.E., Schnack, H.G., van der Linden, J.A.et al.Brain volume changes in first-episode schizophrenia: a 1-year follow-up study. Arch Gen Psychiatry. 2002; 59: 10021010.CrossRefGoogle ScholarPubMed
Crossley NA, Mechelli A, Fusar-Poli P, Broome MR, Matthiasson P, Johns LC, et al. Superior temporal lobe dysfunction and fronto-temporal dysconnectivity in subjects at risk of psychosis and in first-episode psychosis. Hum Brain Mapp 2009;30(12):4129–37.CrossRefGoogle Scholar
Fusar-Poli, P., Perez, J., Broome, M., Borgwardt, S., Placentino, A., Caverzasi, E.et al.Neurofunctional correlates of vulnerability to psychosis: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2007; 31: 465484.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Allen, P., McGuire, P.Neuroimaging studies of the early stages of psychosis: a critical review. Eur Psychiatry. 2008; 23: 237244.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Byrne, M., Valmaggia, L., Day, F., Tabraham, P., Johns, L.et al.Social dysfunction preducts two years clinical outcomes in people at ultrahigh risk for psychosis. J Psychiatr Res. 2009; 44: 294301.CrossRefGoogle Scholar
Fusar-Poli, P., Howes, O.D., Allen, P., Broome, M., Valli, I., Asselin, M.C.et al.Abnormal frontostriatal interactions in people with prodromal signs of psychosis: a multimodal imaging study. Arch Gen Psychiatry. 2010; 67: 683691.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Broome, M.R., Matthiasson, P., Woolley, J.B., Mechelli, A., Johns, L.C.et al.Prefrontal Function at Presentation Directly Related to Clinical Outcome in People at Ultrahigh Risk of Psychosis. Schizophr Bull. 37 1: 2011 189198.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Howes, O.D., Allen, P., Broome, M., Valli, I., Asselin, M.C.et al.Abnormal prefrontal activation directly related to pre-synaptic striatal dopamine dysfunction in people at clinical high risk for psychosis. Mol Psychiatry. 16 1: 2011 6775.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Broome, M., Woolley, J., Johns, L., Tabraham, P., Bramon, E.et al.Altered brain function directly related to structural abnormalities in people at ultra high risk of psychosis: longitudinal VBM-fMRI study. Journal of Psychiatric Research. 45 2: 2011 190198.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Borgwardt, S., Crescini, A., D’Este, G., Kempton, M., Lawrie, S.et al.Neuroanatomical correlates of vulnerability to psychosis: a voxel-based meta-analysis. Neurosci Biobehavioural Review. 35 5: 2011 11751185.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Stone, J.M., Broome, M.R., Valli, I., Mechelli, A., McLean, M.A.et al.Thalamic glutamate levels as a predictor of cortical response during executive functioning in subjects at high risk for psychosis. Arch Gen Psychiatry. 2011.CrossRefGoogle ScholarPubMed
Gao, X.M., Sakai, K., Roberts, R.C., Conley, R.R., Dean, B., Tamminga, C.A.Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am J Psychiatry. 2000; 157: 11411149.CrossRefGoogle ScholarPubMed
Harrison, P.J., Weinberger, D.R.Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry. 2005; 10: 4068.CrossRefGoogle ScholarPubMed
Ho, B.C., Andreasen, N.C., Nopoulos, P., Arndt, S., Magnotta, V., Flaum, M.Progressive structural brain abnormalities and their relationship to clinical outcome: a longitudinal magnetic resonance imaging study early in schizophrenia. Arch Gen Psychiatry. 2003; 60: 585594.CrossRefGoogle Scholar
Hoff, A.L., Svetina, C., Shields, G., Stewart, J., DeLisi, L.E.Ten year longitudinal study of neuropsychological functioning subsequent to a first episode of schizophrenia. Schizophr Res. 2005; 78: 2734.CrossRefGoogle ScholarPubMed
Honey, C.R., Miljkovic, Z., MacDonald, J.F.Ketamine and phencyclidine cause a voltage-dependent block of responses to L-aspartic acid. Neurosci Lett. 1985; 61: 135139.CrossRefGoogle Scholar
Howes, O.D., Montgomery, A.J., Asselin, M., Murray, R., Grasby, P., McGuire, P.Molecular imaging studies of the striatal dopaminergic system in psychosis and predictions for the prodromal phase of psychosis. Br J Psychiatry. s51 2007 s13s18.CrossRefGoogle Scholar
Howes, O., Montgomery, A., Asselin, M., Valli, I., Tabraham, P., Johns, L.et al.Elevated striatal dopamine function linked to prodromal signs of schizophrenia. Arch Gen Psychiatry. 2009; 66: 1320.CrossRefGoogle ScholarPubMed
Kasai, K., Shenton, M.E., Salisbury, D.F., Hirayasu, Y., Lee, C.U., Ciszewski, A.A.et al.Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry. 2003; 160: 156164.CrossRefGoogle ScholarPubMed
Kim, J.S., Kornhuber, H.H., Schmid-Burgk, W., Holzmuller, B.Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis on schizophrenia. Neurosci Lett. 1980; 20: 379382.CrossRefGoogle Scholar
Kubicki, M., Shenton, M.E., Salisbury, D.F., Hirayasu, Y., Kasai, K., Kikinis, R.et al.Voxel-based morphometric analysis of gray matter in first-episode schizophrenia. Neuroimage. 2002; 17: 17111719.CrossRefGoogle ScholarPubMed
Law, A.J., Deakin, J.F.Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses. Neuroreport. 2001; 12: 29712974.CrossRefGoogle ScholarPubMed
Lawrie, S.M., McIntosh, A.M., Hall, J., Owens, D.G., Johnstone, E.C.Brain structure and function changes during the development of schizophrenia: the evidence from studies of subjects at increased genetic risk. Schizophr Bull. 2008; 34: 330340.CrossRefGoogle ScholarPubMed
Mathalon, D.H., Sullivan, E.V., Lim, K.O., Pfefferbaum, A.Progressive brain volume changes and the clinical course of schizophrenia in men: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry. 2001; 58: 148157.CrossRefGoogle ScholarPubMed
Pantelis, C., Velakoulis, D., McGorry, P.D., Wood, S.J., Suckling, J., Phillips, L.J.et al.Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet. 2003; 361: 281288.CrossRefGoogle ScholarPubMed
Phillips, L.J., McGorry, P.D., Yung, A.R., McGlashan, T.H., Cornblatt, B., Klosterkotter, J.Pre-psychotic phase of schizophrenia and related disorders: recent progress and future opportunities. Br J Psychiatry Suppl. 2005; 48: s33s44.CrossRefGoogle Scholar
Pilowsky, L.S., Bressan, R.A., Stone, J.M., Erlandsson, K., Mulligan, R.S., Krystal, J.H.et al.First in vivo evidence of an NMDA receptor deficit in medication-free schizophrenic patients. Mol Psychiatry. 2006; 11: 118119.CrossRefGoogle ScholarPubMed
Shenton, M.E., Dickey, C.C., Frumin, M., McCarley, R.W.A review of MRI findings in schizophrenia. Schizophr Res. 2001; 49: 152.CrossRefGoogle Scholar
Smieskova R, Fusar-Poli P, Allen P, Bendfeldt K, Stieglitz R, Drewe J, et al. Neuroimaging predictors of transition to psychosis: a systematic review andmetaanalysis. Neurosci Biobehav Rev 2010;38(4):1207–22.CrossRefGoogle Scholar
Sporn, A.L., Greenstein, D.K., Gogtay, N., Jeffries, N.O., Lenane, M., Gochman, P.et al.Progressive brain volume loss during adolescence in childhood-onset schizophrenia. Am J Psychiatry. 2003; 160: 21812189.CrossRefGoogle ScholarPubMed
Steel, R.M., Whalley, H.C., Miller, P., Best, J.J., Johnstone, E.C., Lawrie, S.M.Structural MRI of the brain in presumed carriers of genes for schizophrenia, their affected and unaffected siblings. J Neurol Neurosurg Psychiatry. 2002; 72: 455458.Google ScholarPubMed
Stone, J.M., Day, F., Tsagaraki, H., Valli, I., McLean, M.A., Lythgoe, D.J.et al.Glutamate dysfunction in people with prodromal symptoms of psychosis: relationship to gray matter volume. Biol Psychiatry. 66 6: 2009 533539.CrossRefGoogle ScholarPubMed
Suddath, R.L., Christison, G.W., Torrey, E.F., Casanova, M.F., Weinberger, D.R.Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. N Engl J Med. 1990; 322: 789794.CrossRefGoogle Scholar
Sun, D., Phillips, L., Velakoulis, D., Yung, A., McGorry, P., Wood, S.et al.Progressive brain structural changes mapped as psychosis develops in “at-risk” individuals. Schizophr Res. 108 1: 2009 8592.CrossRefGoogle Scholar
Theberge, J., Williamson, K.E., Aoyama, N., Drost, D.J., Manchanda, R., Malla, A.K.et al.Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia. Br J Psychiatry. 2007; 191: 325334.CrossRefGoogle ScholarPubMed
Tibbo, P., Hanstock, C., Valiakalayil, A., Allen, P.3-T proton MRS investigation of glutamate and glutamine in adolescents at high genetic risk for schizophrenia. Am J Psychiatry. 2004; 161: 11161118.CrossRefGoogle ScholarPubMed
Trzesniak, C., Oliveira, I.R., Kempton, M.J., Galvão-de Almeida, A., Chagas, M.H., Ferrari, M.C.et al.Are cavum septum pellucidum abnormalities more common in schizophrenia spectrum disorders? A systematic review and meta-analysis. Schizophr Res. 2011; 125: 112.CrossRefGoogle ScholarPubMed
Valli, I., Stone, J., Mechelli, A., Bhattacharyya, S., Raffin, M., Allen, P.et al.Altered medial temporal activation related to glutamate levels in subjects with prodromal signs of psychosis. Biol Psych. 69 1: 2011 9799.CrossRefGoogle ScholarPubMed
Whalley, H.C., Simonotto, E., Moorhead, W., McIntosh, A., Marshall, I., Ebmeier, K.P.et al.Functional Imaging as a Predictor of Schizophrenia. Biol Psychiatry. 60 5: 2006 454462.CrossRefGoogle ScholarPubMed
Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W., David, A.S., Murray, R.M., Bullmore, E.T.Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry. 2000; 157: 1625.CrossRefGoogle Scholar
Yung, A.R., Phillips, L.J., Yuen, H.P., Francey, S.M., McFarlane, C.A., Hallgren, M.et al.Psychosis prediction: 12-month follow-up of a high risk (“prodromal”) group. Schizophr Res. 2003; 60: 2132.CrossRefGoogle ScholarPubMed
Yung, A.R., Nelson, B., Stanford, C., Simmons, M.B., Cosgrave, E.M., Killackey, E.et al.Validation of “prodromal” criteria to detect individuals at ultra high risk of psychosis: 2 year follow-up. Schizophr Res. 2008; 105: 1017.CrossRefGoogle ScholarPubMed
Submit a response

Comments

No Comments have been published for this article.