Neural Correlates of Emotional Processing in Psychosis Risk and Onset - A Systematic Review and Meta-analysis of FMRI Studies

Overview

Journal Neurosci Biobehav Rev

Specialties Neurology
Psychology
Social Sciences

Date 2021 Mar 16

PMID 33722617

Citations 6

Authors

P B Lukow

A Kiemes

M J Kempton

F E Turkheimer

P McGuire

G Modinos

Affiliations

Soon will be listed here.

Abstract

Aberrant emotion processing is a well-established component of psychotic disorders and is already present at the first episode of psychosis (FEP). However, the role of emotion processing abnormalities in the emergence of psychosis and the underlying neurobiology remain unclear. Here, we systematically reviewed functional magnetic resonance studies that used emotion processing task paradigms in FEP patients, and in people at clinical high-risk for psychosis (CHRp). Image-based meta-analyses with Seed-based d Mapping on available studies (n = 6) were also performed. Compared to controls, FEP patients showed decreased neural responses to emotion, particularly in the amygdala and anterior cingulate cortex. There were no significant differences between CHRp subjects and controls, but a high degree of heterogeneity was identified across studies. The role of altered emotion processing in the early phase of psychosis may be clarified through more homogenous experimental designs, particularly in the CHRp population.

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References

Fusar-Poli P, Nelson B, Valmaggia L, Yung A, McGuire P . Comorbid depressive and anxiety disorders in 509 individuals with an at-risk mental state: impact on psychopathology and transition to psychosis. Schizophr Bull. 2012; 40(1):120-31. PMC: 3885287. DOI: 10.1093/schbul/sbs136. View

Kirby L, Robinson J . Affective mapping: An activation likelihood estimation (ALE) meta-analysis. Brain Cogn. 2015; 118:137-148. DOI: 10.1016/j.bandc.2015.04.006. View

Li H, Chan R, McAlonan G, Gong Q . Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophr Bull. 2009; 36(5):1029-39. PMC: 2930350. DOI: 10.1093/schbul/sbn190. View

Kee K, Green M, Mintz J, Brekke J . Is emotion processing a predictor of functional outcome in schizophrenia?. Schizophr Bull. 2003; 29(3):487-97. DOI: 10.1093/oxfordjournals.schbul.a007021. View

Allott K, Schafer M, Thompson A, Nelson B, Bendall S, Bartholomeusz C . Emotion recognition as a predictor of transition to a psychotic disorder in ultra-high risk participants. Schizophr Res. 2014; 153(1-3):25-31. DOI: 10.1016/j.schres.2014.01.037. View

Yarkoni T, Poldrack R, Nichols T, Van Essen D, Wager T . Large-scale automated synthesis of human functional neuroimaging data. Nat Methods. 2011; 8(8):665-70. PMC: 3146590. DOI: 10.1038/nmeth.1635. View

Lodge D, Behrens M, Grace A . A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci. 2009; 29(8):2344-54. PMC: 2754752. DOI: 10.1523/JNEUROSCI.5419-08.2009. View

Barkl S, Lah S, Harris A, Williams L . Facial emotion identification in early-onset and first-episode psychosis: a systematic review with meta-analysis. Schizophr Res. 2014; 159(1):62-9. DOI: 10.1016/j.schres.2014.07.049. View

Chan R, Li H, Cheung E, Gong Q . Impaired facial emotion perception in schizophrenia: a meta-analysis. Psychiatry Res. 2010; 178(2):381-90. DOI: 10.1016/j.psychres.2009.03.035. View

10.

Hempel A, Hempel E, Schonknecht P, Stippich C, Schroder J . Impairment in basal limbic function in schizophrenia during affect recognition. Psychiatry Res. 2003; 122(2):115-24. DOI: 10.1016/s0925-4927(02)00126-9. View

11.

Heckers S, Konradi C . GABAergic mechanisms of hippocampal hyperactivity in schizophrenia. Schizophr Res. 2014; 167(1-3):4-11. PMC: 4402105. DOI: 10.1016/j.schres.2014.09.041. View

12.

Higgins J, Thompson S . Quantifying heterogeneity in a meta-analysis. Stat Med. 2002; 21(11):1539-58. DOI: 10.1002/sim.1186. View

13.

Linscott R, van Os J . An updated and conservative systematic review and meta-analysis of epidemiological evidence on psychotic experiences in children and adults: on the pathway from proneness to persistence to dimensional expression across mental disorders. Psychol Med. 2012; 43(6):1133-49. DOI: 10.1017/S0033291712001626. View

14.

Tseng H, Roiser J, Modinos G, Falkenberg I, Samson C, McGuire P . Corticolimbic dysfunction during facial and prosodic emotional recognition in first-episode psychosis patients and individuals at ultra-high risk. Neuroimage Clin. 2016; 12():645-654. PMC: 5053033. DOI: 10.1016/j.nicl.2016.09.006. View

15.

Miller T, McGlashan T, Rosen J, Cadenhead K, Cannon T, Ventura J . Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophr Bull. 2004; 29(4):703-15. DOI: 10.1093/oxfordjournals.schbul.a007040. View

16.

Berge D, Carmona S, Salgado P, Rovira M, Bulbena A, Vilarroya O . Limbic activity in antipsychotic naïve first-episode psychotic subjects during facial emotion discrimination. Eur Arch Psychiatry Clin Neurosci. 2013; 264(4):271-83. DOI: 10.1007/s00406-013-0465-5. View

17.

Dugre J, Bitar N, Dumais A, Potvin S . Limbic Hyperactivity in Response to Emotionally Neutral Stimuli in Schizophrenia: A Neuroimaging Meta-Analysis of the Hypervigilant Mind. Am J Psychiatry. 2019; 176(12):1021-1029. DOI: 10.1176/appi.ajp.2019.19030247. View

18.

Muller V, Cieslik E, Laird A, Fox P, Radua J, Mataix-Cols D . Ten simple rules for neuroimaging meta-analysis. Neurosci Biobehav Rev. 2017; 84:151-161. PMC: 5918306. DOI: 10.1016/j.neubiorev.2017.11.012. View

19.

Klosterkotter J, Hellmich M, Steinmeyer E, Schultze-Lutter F . Diagnosing schizophrenia in the initial prodromal phase. Arch Gen Psychiatry. 2001; 58(2):158-64. DOI: 10.1001/archpsyc.58.2.158. View

20.

Smith S, Nichols T . Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2008; 44(1):83-98. DOI: 10.1016/j.neuroimage.2008.03.061. View