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A critical overview of emotion processing assessment in non-affective and affective psychoses

Published online by Cambridge University Press:  15 February 2024

Irene Gorrino
Affiliation:
IUSS Cognitive Neuroscience (ICoN) Center, Scuola Universitaria Superiore IUSS, Pavia, Italy
Maria Gloria Rossetti
Affiliation:
Section of Psychiatry, Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy UOC Psychiatry, Azienda Ospedaliera Universitaria Integrata (AOUI), Verona, Italy
Francesca Girelli
Affiliation:
UOC Psychiatry, Azienda Ospedaliera Universitaria Integrata (AOUI), Verona, Italy
Marcella Bellani
Affiliation:
Section of Psychiatry, Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
Cinzia Perlini*
Affiliation:
Section of Clinical Psychology, Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
Giulia Mattavelli
Affiliation:
IUSS Cognitive Neuroscience (ICoN) Center, Scuola Universitaria Superiore IUSS, Pavia, Italy Cognitive Neuroscience Laboratory of Pavia Institute, Istituti Clinici Scientifici Maugeri IRCCS, Pavia, Italy
*
Corresponding author: Cinzia Perlini; Email: cinzia.perlini@univr.it
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Abstract

Aims

Patients with affective and non-affective psychoses show impairments in both the identification and discrimination of facial affect, which can significantly reduce their quality of life. The aim of this commentary is to present the strengths and weaknesses of the available instruments for a more careful evaluation of different stages of emotion processing in clinical and experimental studies on patients with non-affective and affective psychoses.

Methods

We reviewed the existing literature to identify different tests used to assess the ability to recognise (e.g. Ekman 60-Faces Test, Facial Emotion Identification Test and Penn Emotion Recognition Test) and to discriminate emotions (e.g. Face Emotion Discrimination Test and Emotion Differentiation Task).

Results

The current literature revealed that few studies combine instruments to differentiate between different levels of emotion processing disorders. The lack of comprehensive instruments that integrate emotion recognition and discrimination assessments prevents a full understanding of patients’ conditions.

Conclusions

This commentary underlines the need for a detailed evaluation of emotion processing ability in patients with non-affective and affective psychoses, to characterise the disorder at early phases from the onset of the disease and to design rehabilitation treatments.

Type
Epidemiology for Behavioural Neurosciences
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2024. Published by Cambridge University Press.

Social cognition refers to the mental operations underpinning social interactions, including the perception, encoding, storage, retrieval and regulation of information about oneself and others (Barkl et al., Reference Barkl, Lah, Harris and Williams2014; Brothers, Reference Brothers1990; Gao et al., Reference Gao, Zhao, Liu, Liu, Yang and Xu2021; Green et al., Reference Green, Horan and Lee2015, Reference Green, Penn, Bentall, Carpenter, Gaebel, Gur, Kring, Parl, Sileverstien and Heinssen2008). It is a multifaceted construct entailing five main subdomains: theory of mind (the ability to infer other people’s intentions, inclinations and beliefs), social perception (the identification of social context, roles and rules), attributional bias (the tendency to attribute causes of events to external situations or other’s actions), social knowledge (the awareness of roles, rules and goals that characterise social situations and guide social interactions) and emotion processing (the ability to correctly perceive and use emotions) (Green et al., Reference Green, Penn, Bentall, Carpenter, Gaebel, Gur, Kring, Parl, Sileverstien and Heinssen2008). These processes require the ability to infer the emotions and thoughts of others (Green et al., Reference Green, Horan and Lee2015). To do so, critical information is provided by facial expressions (Barkl et al., Reference Barkl, Lah, Harris and Williams2014; Fusar-Poli et al., Reference Fusar-Poli, Placentino, Carletti, Landi, Allen, Surguladze, Benedetti, Abbamonte, Gasparotti, Barale, Perez, McGuire and Politi2009), which convey emotional states and influence the generation and regulation of emotions and behaviour in response to these signals; thus, the accurate reading of expressions is crucial for affective communication and emotional bonding (Ekman, Reference Ekman1993).

A link has been established between deficits in facial emotion recognition, social and emotional functioning (Yoo and Noyes, Reference Yoo and Noyes2016), which not only contribute to the presence of mood alterations (Oldehinkel et al., Reference Oldehinkel, Hartman, Van Oort and Nederhof2015; Vrijen et al., Reference Vrijen, Hartman and Oldehinkel2016) but also have negative implications for subsequent treatments (Shiroma et al., Reference Shiroma, Thuras, Johns and Lim2014). Indeed, several mental disorders, including schizophrenia (Addington et al., Reference Addington, Saeedi and Addington2006; Green et al., Reference Green, Horan and Lee2015) and psychotic disorders (Benito et al., Reference Benito, Lahera, Herrera, Muncharaz, Benito, Fernández-Liria and Montes2013; Ulusoy et al., Reference Ulusoy, Gülseren, Özkan and Bilen2020), are characterised by deficits in facial emotion recognition.

There is robust evidence that people with affective and non-affective psychoses show impairments in emotion perception (Edwards et al., Reference Edwards, Jackson and Pattison2002; Kohler et al., Reference Kohler, Walker, Martin, Healey and Moberg2010; Priyesh et al., Reference Priyesh, Suryavanshi, Sasidharan, Bhandary, Behere and Nayak2022; Rocca et al., Reference Rocca, Heuvel, Caetano and Lafer2009), experience reduced interpersonal skills (Pinkham et al., Reference Pinkham, Penn, Perkins, Graham and Siegel2007) and report social and work difficulties (Addington et al., Reference Addington, Saeedi and Addington2006; Kee et al., Reference Kee, Green, Mintz and Brekke2003). A recent meta-analysis revealed a specific distinction between the two patient groups. Indeed, individuals with affective psychosis demonstrated a greater ability to identify emotional facial expressions compared to non-affective psychosis patients, in particular for emotions of anger, fear and sadness (De Prisco et al., Reference De Prisco, Oliva, Fico, Montejo, Possidente, Bracco, Fortea, Anmella, Hidalgo-Mazzei, Fornaro, de Bartolomeis, Serretti, Murru, Vieta and Radua2023). Importantly, the severity of psychotic symptoms correlates with deficits in emotion processing (Kohler et al., Reference Kohler, Bilker, Hagendoorn, Gur and Gur2000; Schneider et al., Reference Schneider, Gur, Gur and Shtasel1995), which can be even present in healthy individuals at higher risk of developing schizophrenia based on risk factors such as schizotypal personality traits or genetic susceptibility (Kee et al., Reference Kee, Horan, Mintz and Green2004; Van’t Wout et al., Reference Van’t Wout, Aleman, Kessels, Larøi and Kahn2004). Moreover, first episode psychosis patients, in particular non-affective patients, already showed lower ability to label positive and negative emotional prosody, suggesting early disruption in their emotion recognition system (Caletti et al., Reference Caletti, Delvecchio, Andreella, Finos, Perlini, Tavano, Lasalvia, Bonetto, Cristofalo, Lamonaca, Ceccato, Pileggi, Mazzi, Santonastaso, Ruggeri, Bellani and Brambilla2018). Emotional dysfunction may, therefore, represent an index of early signs of the disease (Seiferth et al., Reference Seiferth, Pauly, Habel, Kellermann, Shah, Ruhrmann and Kircher2008), while strengthening the emotion recognition ability may improve prevention and intervention strategies (Comparelli et al., Reference Comparelli, Corigliano, De Carolis, Mancinelli, Trovini, Ottavi, Dehning, Tatarelli, Brugnoli and Girardi2013).

As facial emotion recognition skills can be enhanced by training (Combs et al., Reference Combs, Adams, Penn, Tiegreen and Stem2007; Wölwer et al., Reference Wölwer, Frommann, Halfmann, Piaszek, Streit and Gaebel2005), much work has been done to characterise the deficit, its relationship to symptoms and neural basis (Marwick and Hall, Reference Marwick and Hall2008). Structural and functional anomalies have been found in the insula and amygdala (Crespo-Facorro et al., Reference Crespo-Facorro, Kim, Andreasen, O’Leary, Bockholt and Magnotta2000; Honea et al., Reference Honea, Crow, Passingham and Mackay2005; Wright et al., Reference Wright, Rabe-Hesketh, Woodruff, David, Murray and Bullmore2000), with evidence of hypoactivation in patients with schizophrenia for fearful compared to neutral faces (Aleman and Kahn, Reference Aleman and Kahn2005; Delvecchio et al., Reference Delvecchio, Sugranyes and Frangou2012). This finding suggests that an undifferentiated amygdala response to fearful and neutral faces may hinder their discrimination and lead to misattribution of fear depending on the context (Marwick and Hall, Reference Marwick and Hall2008). In contrast, patients with affective psychosis show increased activation of the amygdala and hippocampus, consistent with the notion of greater arousal responses to emotional stimuli (Critchley et al., Reference Critchley, Rotshtein, Nagai, O’Doherty, Mathias and Dolan2005; Delvecchio et al., Reference Delvecchio, Sugranyes and Frangou2012; Santos et al., Reference Santos, Mier, Kirsch and Meyer-Lindenberg2010), but also better contextual appraisal compared to schizophrenia patients (Delvecchio et al., Reference Delvecchio, Sugranyes and Frangou2012; Gerdes et al., Reference Gerdes, Wieser, Mühlberger, Weyers, Alpers, Plichta, Breuer and Pauli2010). In addition, increased pulvinar activation in affective psychosis has been found, suggesting a greater focus on emotionally salient stimuli from early stages of visual processing (Pessoa and Adolphs, Reference Pessoa and Adolphs2010), whereas the emotional dysregulation may be related to deficit of grey matter volume in subgenual anterior cingulate cortex (Maggioni et al., Reference Maggioni, Crespo-Facorro, Nenadic, Benedetti, Gaser, Sauer, Roiz-Santianez, Poletti, Marinelli, Bellani, Perlini, Ruggeri, Altamura, Diwadkar and Brambilla2017). Taken together, these findings highlight the complex interplay between neural processes, emotional responses and contextual appraisal in individuals with different forms of psychosis. The role of the amygdala in discriminating and attributing emotions, as well as the increased activation observed in affective psychosis, highlights its potential role in the enhance patients’ experience of fear and arousal (Marwick and Hall, Reference Marwick and Hall2008; Wright et al., Reference Wright, Rabe-Hesketh, Woodruff, David, Murray and Bullmore2000). On the other hand, findings of reduce volume in limbic regions such as the insula and cingulate cortex may underlie difficulties in adaptive responses to emotional stimuli even at the onset of symptoms (Crespo-Facorro et al., Reference Crespo-Facorro, Kim, Andreasen, O’Leary, Bockholt and Magnotta2000; Maggioni et al., Reference Maggioni, Crespo-Facorro, Nenadic, Benedetti, Gaser, Sauer, Roiz-Santianez, Poletti, Marinelli, Bellani, Perlini, Ruggeri, Altamura, Diwadkar and Brambilla2017). A better understanding of regional variations and their relation to patients’ symptoms is relevant to shed light on the mechanisms underlying emotional deficits and to offer potential paths for tailored interventions in individuals with psychosis.

Notably, emotion processing involves several stages, which are measured by different tasks. Four main levels can be identified: i) unconscious processing refers to stimuli which are potentially accessible to consciousness but are processed in absence of awareness because they are below the threshold of perception (Dehaene et al., Reference Dehaene, Changeux, Naccache, Sackur and Sergent2006; Mattavelli et al., Reference Mattavelli, Pisoni, Romero Lauro, Marino, Bonomi, Rosanova and Papagno2019), ii) perceptual sensitivity is the individual threshold at which stimuli can be differentiated from noise or other stimuli (Pessoa et al., Reference Pessoa, Japee and Ungerleider2005), iii) the discrimination requires to distinguish between expressions and iv) recognition further requires to identify the target emotion (Adolphs et al., Reference Adolphs, Damasio, Tranel, Cooper and Damasio2000). The first two levels are tested with forced-choice tasks and using very brief presentation of stimuli (e.g. 10–30 ms target). Discrimination and recognition are instead assessed by identification tasks. While sensitivity depends on sensory and visuospatial processes, emotion recognition also requires the ability to label the correct emotion among several alternatives (Haxby et al., Reference Haxby, Hoffman and Gobbini2002). As the neural pathways underlying perceptual processing and emotion recognition are partially distinct and can be selectively impaired in different neuropsychiatric conditions (Mattavelli et al., Reference Mattavelli, Barvas, Longo, Zappini, Ottaviani, Malaguti and Papagno2021; Tamietto and De Gelder, Reference Tamietto and De Gelder2010), it is necessary to assess whether impairments occur at early perceptual processing or/and recognition of emotions.

This commentary aims at presenting an overview of the strengths and weaknesses of the available instruments assessing the different stages of facial emotion processing in patients with non-affective and affective psychoses. Since the deficits in social cognition domain are related to psychotic symptoms and quality of life, a deeper characterisation of emotion processing capacity is crucial for a better understanding of the pathologies and to promote personalised interventions.

Up to date, most studies have used emotion recognition tests in schizophrenia (Addington et al., Reference Addington, Penn, Woods, Addington and Perkins2008; Pinkham et al., Reference Pinkham, Penn, Perkins, Graham and Siegel2007) and bipolar disorder (Benito et al., Reference Benito, Lahera, Herrera, Muncharaz, Benito, Fernández-Liria and Montes2013; Ulusoy et al., Reference Ulusoy, Gülseren, Özkan and Bilen2020). The most reported are the Ekman 60-Faces Test (EK-60F; Young et al., Reference Young, Perrett, Calder, Sprengelmeyer and Ekman2002), the Facial Emotion Identification Test (FEIT; Kerr and Neale, Reference Kerr and Neale1993) and the Penn Emotion Recognition Test (ER-40; Kohler et al., Reference Kohler, Turner, Bilker, Brensinger, Siegel, Kanes and Gur2003). In the former, participants are shown a series of 60 black-and-white photographs of male and female faces expressing one of six basic emotions (surprise, happiness, fear, disgust, anger and sadness) and are required to associate the correct label to each emotion. The reliability and validity of this instrument have been demonstrated in several studies (Róza et al., Reference Róza, Kálmán, Ko, Ngay, Fiáth, Magi, Eisinger and Oláh2012). The FEIT similarly uses the stimuli developed by Ekman and Friesen (Reference Ekman and Friesen1976) and Izard (Reference Izard1971) but presents only 19 faces, 15 expressing negative (anger, sadness, fear and shame) and 4 expressing positive emotions (happiness and surprise). The FEIT has established psychometric properties (Dougherty et al., Reference Dougherty, Bartlett and Izard1974; Feinberg et al., Reference Feinberg, Rifkin, Schaffer and Walker1986; Zuroff and Colussy, Reference Zuroff and Colussy1986) and includes a control task to rule out the possibility that the poor performance of patients generally reflects cognitive impairments (Chapman and Chapman, Reference Chapman and Chapman1973, Reference Chapman and Chapman1978; Oltmanns and Neale, Reference Oltmanns and Neale1978). It has been validated for Korean (Bahk et al., Reference Bahk, Jang, Lee and Choi2015) and Chinese (Lo and Siu, Reference Lo and Siu2018) populations, but no normative data are currently available for the European and South American populations, which limits its clinical use. In contrast, the EK-60F has been validated in Korea (Kim et al., Reference Kim, Kwon, Jung, Kim, Cho, Kim and Choi2017) and Italy (Dodich et al., Reference Dodich, Cerami, Canessa, Crespi, Marcone, Arpone, Realmuto and Cappa2014). Finally, the ER-40 includes 40 colour-posed facial expressions of four emotions (anger, sadness, happiness or fear) with high and low intensity, as well as neutral (Kohler et al., Reference Kohler, Turner, Bilker, Brensinger, Siegel, Kanes and Gur2003), and participants are instructed to identify the expressed emotion among five possible choices.

Instead, the most reported test for assessing emotion discrimination ability is the Face Emotion Discrimination Test (FEDT), which was developed by Kerr and Neale (Reference Kerr and Neale1993) in parallel with the FEIT. It uses 30 pairs of stimuli from the Izard (1971) set, and subjects are asked to decide whether the same or different emotions are presented. Like the FEIT, the FEDT is validated with established psychometric properties (Dougherty et al., Reference Dougherty, Bartlett and Izard1974; Feinberg et al., Reference Feinberg, Rifkin, Schaffer and Walker1986; Kerr and Neale, Reference Kerr and Neale1993; Zuroff and Colussy, Reference Zuroff and Colussy1986), although normative data are currently available only for USA and Korean (Bahk et al., Reference Bahk, Jang, Lee and Choi2015) populations. Another test is the Emotion Differentiation Task (EMODIFF; Kohler et al., Reference Kohler, Bilker, Hagendoorn, Gur and Gur2000), in which participants are asked to differentiate the intensity of emotions shown in two side-by-side faces of the same person.

Few previous studies have combined these instruments and reported that both discrimination and recognition were impaired in patients and in high-risk individuals for psychosis (Addington et al., Reference Addington, Penn, Woods, Addington and Perkins2008; Benito et al., Reference Benito, Lahera, Herrera, Muncharaz, Benito, Fernández-Liria and Montes2013; Comparelli et al., Reference Comparelli, Corigliano, De Carolis, Mancinelli, Trovini, Ottavi, Dehning, Tatarelli, Brugnoli and Girardi2013; Ulusoy et al., Reference Ulusoy, Gülseren, Özkan and Bilen2020), suggesting a general impairment involving early stage of processing. On the other hand, studies with experimental paradigms assessing unconscious emotion processing, at behavioural and brain activity level, reported inconsistent data on early automatic stages, which resulted impaired or preserved in different samples of patients with psychosis (Brennan et al., Reference Brennan, Harris and Williams2014; Gruber et al., Reference Gruber, Siegel, Purcell, Earls, Cooper and Barrett2016; Williams et al., Reference Williams, Whitford, Nagy, Flynn, Harris, Silverstein and Gordon2009). The independency vs hierarchical dependency of the different stages including unconscious processing, early visual processing, recognition and labelling of emotions is a debated issue (Barrett et al., Reference Barrett, Lindquist and Gendron2007; Kring et al., Reference Kring, Siegel and Barrett2014). Hierarchical models propose a feed-forward propagation of signals from sensory to higher-level cortical areas, with the latter projecting feedback on early processing areas to support coherent representations throughout top-down modulation. Other models hypothesise the presence of independent pathways for conscious and unconscious processing, with signal diverging from early stages and involving distinct cortical and subcortical neural networks (Dehaene and Changeux, Reference Dehaene and Changeux2011; Tamietto and De Gelder, Reference Tamietto and De Gelder2010). Within this framework, refining patients’ assessment has significant theoretical and translational implications. Individual perceptual sensitivity and unconscious processing can be evaluated with backward masking (Williams et al., Reference Williams, Whitford, Nagy, Flynn, Harris, Silverstein and Gordon2009) or continuous flash suppression (CFS) paradigms (Gruber et al., Reference Gruber, Siegel, Purcell, Earls, Cooper and Barrett2016) to clarify whether emotional dysfunction is related to a deficit in early processing of salience and elucidate the role of anomalies in the recurrent interactions between visual and higher-level associative areas for access to consciousness (Dehaene and Changeux, Reference Dehaene and Changeux2011; Del Cul et al., Reference Del Cul, Dehaene and Leboyer2006).

In conclusion, emotion processing involves multiple stages, from unconscious processing to recognition and discrimination of emotions. Different tests, summarised in Table 1, have been developed to assess these stages. Although impairments have been observed in patients with non-affective and affective psychoses, the precise nature of these deficits remains a subject of debate. Therefore, refining patients’ assessment is crucial for a better characterisation of deficits in both affective and non-affective psychosis, which could be used to modulate new cognitive remediation and social skills training interventions aimed at enhancing emotion processing skills and improving effective interaction in social contexts.

Table 1. Characteristics of tasks used to assess the different stages of emotion processing in psychosis

Availability of data and materials

All data used to write this paper are in the reference list.

Financial support

This study was partially supported by a grant from the Italian Ministry of Health (GR-2016-02361283 to GM and CP).

Competing interests

None.

References

Addington, J, Penn, D, Woods, SW, Addington, D and Perkins, DO (2008) Facial affect recognition in individuals at clinical high risk for psychosis. The British Journal of Psychiatry 192, 6768.CrossRefGoogle ScholarPubMed
Addington, J, Saeedi, H and Addington, D (2006) Facial affect recognition: A mediator between cognitive and social functioning in psychosis? Schizophrenia Research 85, 142150.CrossRefGoogle ScholarPubMed
Adolphs, R, Damasio, H, Tranel, D, Cooper, G and Damasio, AR (2000) A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. The Journal of Neuroscience 20, 26832690.CrossRefGoogle ScholarPubMed
Aleman, A and Kahn, RS (2005) Strange feelings: Do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Progress in Neurobiology 77, 283298.Google ScholarPubMed
Bahk, YC, Jang, SK, Lee, JY and Choi, KH (2015) Korean facial emotion recognition tasks for schizophrenia research. Psychiatry Investigation 12, .CrossRefGoogle ScholarPubMed
Barkl, SJ, Lah, S, Harris, AW and Williams, LM (2014) Facial emotion identification in early-onset and first-episode psychosis: A systematic review with meta-analysis. Schizophrenia Research 159, 6269.CrossRefGoogle ScholarPubMed
Barrett, LF, Lindquist, KA and Gendron, M (2007) Language as context for the perception of emotion. Trends in Cognitive Sciences 11, 327332.CrossRefGoogle ScholarPubMed
Benito, A, Lahera, G, Herrera, S, Muncharaz, R, Benito, G, Fernández-Liria, A and Montes, JM (2013) Deficits in recognition, identification, and discrimination of facial emotions in patients with bipolar disorder. Brazilian Journal of Psychiatry 35, 435438.CrossRefGoogle ScholarPubMed
Brennan, AM, Harris, AWF and Williams, LM (2014) Neural processing of facial expressions of emotion in first onset psychosis. Psychiatry Research 219, 477485.CrossRefGoogle ScholarPubMed
Brothers, L (1990) The neural basis of primate social communication. Motivation and Emotion 14, 8191.CrossRefGoogle Scholar
Caletti, E, Delvecchio, G, Andreella, A, Finos, L, Perlini, C, Tavano, A, Lasalvia, A, Bonetto, C, Cristofalo, D, Lamonaca, D, Ceccato, E, Pileggi, F, Mazzi, F, Santonastaso, P, Ruggeri, M, Bellani, M, Brambilla, P and GET UP Group (2018) Prosody abilities in a large sample of affective and non-affective first episode psychosis patients. Comprehensive Psychiatry 86, 3138.CrossRefGoogle Scholar
Chapman, LJ and Chapman, JP (1973) Problems in the measurement of cognitive deficit. Psychological Bulletin 79, 380383.CrossRefGoogle ScholarPubMed
Chapman, LJ and Chapman, JP (1978) The measurement of differential deficit. Journal of Psychiatric Research 14, 303311.CrossRefGoogle ScholarPubMed
Combs, DR, Adams, SD, Penn, DL, Tiegreen, J and Stem, P (2007) Social Cognition and Interaction Training (SCIT) for inpatients with schizophrenia spectrum disorders: Preliminary findings. Schizophrenia Research 91, 112116.CrossRefGoogle ScholarPubMed
Comparelli, A, Corigliano, V, De Carolis, A, Mancinelli, I, Trovini, G, Ottavi, G, Dehning, J, Tatarelli, R, Brugnoli, R and Girardi, P (2013) Emotion recognition impairment is present early and is stable throughout the course of schizophrenia. Schizophrenia Research 143, 6569.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Kim, JJ, Andreasen, NC, O’Leary, DS, Bockholt, HJ and Magnotta, V (2000) Insular cortex abnormalities in schizophrenia: A structural magnetic resonance imaging study of first-episode patients. Schizophrenia Research 46, 3543.CrossRefGoogle ScholarPubMed
Critchley, HD, Rotshtein, P, Nagai, Y, O’Doherty, J, Mathias, CJ and Dolan, RJ (2005) Activity in the human brain predicting differential heart rate responses to emotional facial expressions. NeuroImage 24, 751762.CrossRefGoogle ScholarPubMed
Dehaene, S and Changeux, JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70, 200227.CrossRefGoogle ScholarPubMed
Dehaene, S, Changeux, JP, Naccache, L, Sackur, J and Sergent, C (2006) Conscious, preconscious, and subliminal processing: A testable taxonomy. Trends in Cognitive Sciences 10, 204211.CrossRefGoogle ScholarPubMed
Del Cul, A, Dehaene, S and Leboyer, M (2006) Preserved subliminal processing and impaired conscious access in schizophrenia. Archives of General Psychiatry 63, 13131323.CrossRefGoogle ScholarPubMed
Delvecchio, G, Sugranyes, G and Frangou, S (2012) Evidence of diagnostic specificity in the neural correlates of facial affect processing in bipolar disorder and schizophrenia: A meta-analysis of functional imaging studies. Psychological Medicine 43, 553569.CrossRefGoogle ScholarPubMed
De Prisco, M, Oliva, V, Fico, G, Montejo, L, Possidente, C, Bracco, L, Fortea, L, Anmella, G, Hidalgo-Mazzei, D, Fornaro, M, de Bartolomeis, A, Serretti, A, Murru, A, Vieta, E and Radua, J (2023) Differences in facial emotion recognition between bipolar disorder and other clinical populations: A systematic review and meta-analysis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 127, .CrossRefGoogle ScholarPubMed
Dodich, A, Cerami, C, Canessa, N, Crespi, C, Marcone, A, Arpone, M, Realmuto, S and Cappa, SF (2014) Emotion recognition from facial expressions: A normative study of the Ekman 60-Faces Test in the Italian population. Neurological Sciences 35, 10151021.CrossRefGoogle ScholarPubMed
Dougherty, FE, Bartlett, ES and Izard, CE (1974) Response of schizophrenics to expressions of the fundamental emotions. Journal of Clinical Psychology 30, 243246.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Edwards, J, Jackson, HJ and Pattison, PE (2002) Emotion recognition via facial expression and affective prosody in schizophrenia: A methodological review. Clinical Psychology Review 22, 789832.CrossRefGoogle ScholarPubMed
Ekman, P (1993) Facial expression and emotion. American Psychologist 48, .CrossRefGoogle ScholarPubMed
Ekman, P and Friesen, WV (1976) Pictures of Facial Affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Feinberg, TE, Rifkin, A, Schaffer, C and Walker, E (1986) Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry 43, 276279.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Placentino, A, Carletti, F, Landi, P, Allen, P, Surguladze, S, Benedetti, F, Abbamonte, M, Gasparotti, R, Barale, F, Perez, J, McGuire, P and Politi, P (2009) Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience 34, 418432.Google ScholarPubMed
Gao, Z, Zhao, W, Liu, S, Liu, Z, Yang, C and Xu, Y (2021) Facial emotion recognition in schizophrenia. Frontiers in Psychiatry 12, .CrossRefGoogle ScholarPubMed
Gerdes, AB, Wieser, MJ, Mühlberger, A, Weyers, P, Alpers, GW, Plichta, MM, Breuer, F and Pauli, P (2010) Brain activations to emotional pictures are differentially associated with valence and arousal ratings. Frontiers in Human Neuroscience 4, .CrossRefGoogle ScholarPubMed
Green, MF, Horan, WP and Lee, J (2015) Social cognition in schizophrenia. Nature Reviews Neuroscience 16, 620631.CrossRefGoogle ScholarPubMed
Green, MF, Penn, DL, Bentall, R, Carpenter, WT, Gaebel, W, Gur, RC, Kring, AM, Parl, S, Sileverstien, SM and Heinssen, R (2008) Social cognition in schizophrenia: An NIMH workshop on definitions, assessment, and research opportunities. Schizophrenia Bulletin 34, 12111220.CrossRefGoogle ScholarPubMed
Gruber, J, Siegel, EH, Purcell, AL, Earls, HA, Cooper, G and Barrett, LF (2016) Unseen positive and negative affective information influences social perception in bipolar disorder and healthy adults. Journal of Affective Disorders 192, 191198.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA and Gobbini, MI (2002) Human neural systems for face recognition and social communication. Biological Psychiatry 51, 5967.CrossRefGoogle ScholarPubMed
Honea, R, Crow, TJ, Passingham, D and Mackay, CE (2005) Regional deficits in brain volume in schizophrenia: A meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 162, 22332245.CrossRefGoogle ScholarPubMed
Izard, CE (1971) The Face of Emotion. New York: Appleton-Century-Crofts.Google Scholar
Kee, KS, Green, MF, Mintz, J and Brekke, JS (2003) Is emotion processing a predictor of functional outcome in schizophrenia? Schizophrenia Bulletin 29, 487497.CrossRefGoogle ScholarPubMed
Kee, KS, Horan, WP, Mintz, J and Green, MF (2004) Do the siblings of schizophrenia patients demonstrate affect perception deficits? Schizophrenia Research 67, 8794.CrossRefGoogle ScholarPubMed
Kerr, SL and Neale, JM (1993) Emotion perception in schizophrenia: Specific deficit or further evidence of generalized poor performance? Journal of Abnormal Psychology 102, .CrossRefGoogle ScholarPubMed
Kim, SM, Kwon, YJ, Jung, SY, Kim, MJ, Cho, YS, Kim, HT and Choi, JS (2017) Development of the Korean facial emotion stimuli: Korea university facial expression collection 2nd edition. Frontiers in Psychology 8, .CrossRefGoogle ScholarPubMed
Kohler, CG, Bilker, W, Hagendoorn, M, Gur, RE and Gur, RC (2000) Emotion recognition deficit in schizophrenia: Association with symptomatology and cognition. Biological Psychiatry 48, 127136.CrossRefGoogle ScholarPubMed
Kohler, CG, Turner, TH, Bilker, WB, Brensinger, CM, Siegel, SJ, Kanes, SJ and Gur, RC (2003) Facial emotion recognition in schizophrenia: Intensity effects and error pattern. American Journal of Psychiatry 160, 17681774.CrossRefGoogle ScholarPubMed
Kohler, CG, Walker, JB, Martin, EA, Healey, KM and Moberg, PJ (2010) Facial emotion perception in schizophrenia: A meta-analytic review. Schizophrenia Bulletin 36, 10091019.CrossRefGoogle ScholarPubMed
Kring, AM, Siegel, EH and Barrett, LF (2014) Unseen affective faces influence person perception judgments in schizophrenia. Clinical Psychological Science 2, 443454.CrossRefGoogle ScholarPubMed
Lo, PM and Siu, AM (2018) Assessing social cognition of persons with schizophrenia in a Chinese population: A pilot study. Frontiers in Psychiatry 8, .CrossRefGoogle Scholar
Maggioni, E, Crespo-Facorro, B, Nenadic, I, Benedetti, F, Gaser, C, Sauer, H, Roiz-Santianez, R, Poletti, S, Marinelli, V, Bellani, M, Perlini, C, Ruggeri, M, Altamura, CA, Diwadkar, VA, Brambilla, P and ENPACT group (2017) Common and distinct structural features of schizophrenia and bipolar disorder: The European Network on Psychosis, Affective disorders and Cognitive Trajectory (ENPACT) study. PLoS One 12, .CrossRefGoogle ScholarPubMed
Marwick, K and Hall, J (2008) Social cognition in schizophrenia: A review of face processing. British Medical Bulletin 88, 4358.CrossRefGoogle ScholarPubMed
Mattavelli, G, Barvas, E, Longo, C, Zappini, F, Ottaviani, D, Malaguti, MC and Papagno, C (2021) Facial expressions recognition and discrimination in Parkinson’s disease. Journal of Neuropsychology 15, 4668.CrossRefGoogle ScholarPubMed
Mattavelli, G, Pisoni, A, Romero Lauro, LJ, Marino, BF, Bonomi, M, Rosanova, M and Papagno, C (2019) TMS-EEG approach unveils brain mechanisms underlying conscious and unconscious face perception. Brain Stimulation 12, 10101019.CrossRefGoogle ScholarPubMed
Oldehinkel, AJ, Hartman, CA, Van Oort, FV and Nederhof, E (2015) Emotion recognition specialization and context‐dependent risk of anxiety and depression in adolescents. Brain and Behavior 5, .CrossRefGoogle ScholarPubMed
Oltmanns, TF and Neale, JM (1978) Abstraction and schizophrenia: Problems in psychological deficit research. Progress in Experimental Personality Research 8, 197243.Google ScholarPubMed
Pessoa, L and Adolphs, R (2010) Emotion processing and the amygdala: From a ‘low road’ to ‘many roads’ of evaluating biological significance. Nature Reviews Neuroscience 11, 773783.CrossRefGoogle ScholarPubMed
Pessoa, L, Japee, S and Ungerleider, LG (2005) Visual awareness and the detection of fearful faces. Emotion 5, 243247.CrossRefGoogle ScholarPubMed
Pinkham, AE, Penn, DL, Perkins, DO, Graham, KA and Siegel, M (2007) Emotion perception and social skill over the course of psychosis: A comparison of individuals “at-risk” for psychosis and individuals with early and chronic schizophrenia spectrum illness. Cognitive Neuropsychiatry 12, 198212.CrossRefGoogle ScholarPubMed
Priyesh, C, Suryavanshi, CA, Sasidharan, A, Bhandary, R, Behere, RV and Nayak, KR (2022) Facial emotion recognition, misattribution, and response time in schizophrenia and bipolar disorder. Neurophysiology 53, 120131.CrossRefGoogle Scholar
Rocca, CCDA, Heuvel, EVD, Caetano, SC and Lafer, B (2009) Facial emotion recognition in bipolar disorder: A critical review. Brazilian Journal of Psychiatry 31, 171180.CrossRefGoogle ScholarPubMed
Róza, S, Kálmán, R, Ko, N, Ngay, H, Fiáth, T, Magi, A, Eisinger, A and Oláh, A (2012) Assessment of facial expression: Reliability and validity of the Ekman 60 Faces Test. Pszichológia 32, 229251.Google Scholar
Santos, A, Mier, D, Kirsch, P and Meyer-Lindenberg, A (2010) Evidence for a general face salience signal in human amygdala. NeuroImage 54, 31113116.CrossRefGoogle ScholarPubMed
Schneider, F, Gur, RC, Gur, RE and Shtasel, DL (1995) Emotional processing in schizophrenia: Neurobehavioral probes in relation to psychopathology. Schizophrenia Research 17, 6775.CrossRefGoogle ScholarPubMed
Seiferth, NY, Pauly, K, Habel, U, Kellermann, T, Shah, NJ, Ruhrmann, S and Kircher, T (2008) Increased neural response related to neutral faces in individuals at risk for psychosis. NeuroImage 40, 289297.CrossRefGoogle ScholarPubMed
Shiroma, PR, Thuras, P, Johns, B and Lim, KO (2014) Emotion recognition processing as early predictor of response to 8‐week citalopram treatment in late‐life depression. International Journal of Geriatric Psychiatry 29, 11321139.CrossRefGoogle ScholarPubMed
Tamietto, M and De Gelder, B (2010) Neural bases of the non-conscious perception of emotional signals. Nature Reviews Neuroscience 11, 697709.CrossRefGoogle ScholarPubMed
Ulusoy, SI, Gülseren, ŞA, Özkan, N and Bilen, C (2020) Facial emotion recognition deficits in patients with bipolar disorder and their healthy parents. General Hospital Psychiatry 65, 914.CrossRefGoogle Scholar
Van’t Wout, M, Aleman, A, Kessels, RP, Larøi, F and Kahn, S (2004) Emotional processing in a non-clinical psychosis-prone sample. Schizophrenia Research 68, 271281.CrossRefGoogle Scholar
Vrijen, C, Hartman, CA and Oldehinkel, AJ (2016) Slow identification of facial happiness in early adolescence predicts onset of depression during 8 years of follow-up. European Child and Adolescent Psychiatry 25, 12551266.CrossRefGoogle ScholarPubMed
Williams, LM, Whitford, TJ, Nagy, M, Flynn, G, Harris, AWF, Silverstein, SM and Gordon, E (2009) Emotion-elicited gamma synchrony in patients with first-episode schizophrenia: A neural correlate of social cognition outcomes. Journal of Psychiatry & Neuroscience 34, 303313.Google ScholarPubMed
Wölwer, W, Frommann, N, Halfmann, S, Piaszek, A, Streit, M and Gaebel, W (2005) Remediation of impairments in facial affect recognition in schizophrenia: Efficacy and specificity of a new training program. Schizophrenia Research 80, 295303.CrossRefGoogle ScholarPubMed
Wright, IC, Rabe-Hesketh, S, Woodruff, PW, David, AS, Murray, RM and Bullmore, ET (2000) Meta-analysis of regional brain volumes in schizophrenia. American Journal of Psychiatry 157, 1625.CrossRefGoogle ScholarPubMed
Yoo, SH and Noyes, SE (2016) Recognition of facial expressions of negative emotions in romantic relationships. Journal of Nonverbal Behavior 40, 112.CrossRefGoogle Scholar
Young, AW, Perrett, D, Calder, A, Sprengelmeyer, R and Ekman, P (2002) Facial expressions of emotion: Stimuli and tests (FEEST). Bury St. Edmunds: Thames Valley Test Company.Google Scholar
Zuroff, DC and Colussy, SA (1986) Emotion recognition in schizophrenic and depressed inpatients. Journal of Clinical Psychology 42, 411416.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
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Table 1. Characteristics of tasks used to assess the different stages of emotion processing in psychosis