Participants

Participants were 100 in-patients from Lublin University Psychiatric Hospital with schizophrenia in remission (diagnosed on the basis of clinical interview according to DSM–IV criteria; American Psychiatric Association, 1994); 50 patients (25 male) were recruited during the first or second episode of illness (≤2 episodes; mean duration of illness=2.0 years (s.d.=1.3)) and 50 (26 male) during later stages of illness (>2 episodes; mean duration of illness=13.2 years (s.d.=6.6)). All patients were clinically stable after 4 weeks of neuroleptic treatment (65% atypical antipsychotics) and were aged between 18 and 60 years. The mean daily dose in chlorpromazine equivalents was 365 mg (s.d.=165).

The 30-item Positive and Negative Syndrome Scale (PANSS; Reference Kay, Opler and FiszbeinKay et al, 1987) was administered to all patients by a trained rater (K. K.-P.) at the time of recruitment (Table 1). Controls were 50 healthy individuals (24 male; mean age=36.8 years (s.d.=13.4)) with no history of psychiatric illness recruited from the non-professional staff at Lublin University Medical School and Lublin Psychiatric Hospital.

Table 1

Demographic and clinical data for the three groups

Variable, mean (s.d.)	Healthy controls	Patients in early stages of schizophreania	Patients with chronic schizophrenia	F (d.f.=2,1)	P
Age, years	36.8 (13.4)	23.1 (4.2)	41.6 (10.3)	38.9	<0.001
Education, years	13.5 (3.0)	12.1 (1.8)	12.3 (3.4)	3.30	0.04
Duration of illness, years	–	2.0 (1.3)	13.2 (6.6)	58.8	<0.001
Number of admissions	–	1.3 (0.7)	4.6 (2.8)	26.6	<0.001
Neuroleptic dose, CPZ equivalents, mg/day	–	365 (165)	383 (131)	0.62	0.53
PANSS score
Positive symptoms	–	11.8 (3.1)	11.7 (3.5)	0.007	0.99
Negative symptoms	–	22.4 (5.6)	26.0 (5.5)	1.42	0.24
General psychopathology	–	33.1 (6.6)	34.6 (6.8)	0.62	0.54
Mood rating	62.8 (15.1)	53.2 (23.2)	56.9 (2.5)	2.91	0.06
BFRT	83.3 (8.1)	77.8 (8.7)	73.2 (9.3)	16.85	<0.001

All participants were right-handed (Reference AnnettAnnett, 1970). Exclusion criteria included the presence of a neurological disorder (e.g. epilepsy, dementia), habitual drug or alcohol misuse and cognitive impairment (a minimum score <24 out of 30 on the Mini-Mental State Examination; Reference Folstein, Folstein and McHughFolstein et al, 1975). Those who had difficulties with vision (including poor acuity and lack of correction) or hearing (threshold greater than 35 dB at any frequency using a free-field voice test; Reference BrowningBrowning, 1998) were also excluded. Informed consent was obtained prior to participation in the study. Approval for the study was obtained from the ethics committee of the Psychiatry Department of Lublin University Medical School. Six patients with schizophrenia who volunteered to take part in the study were not included in the final sample because either they were unable to complete the full set of tests owing to akathisia (three) or agitation (one) or they were discharged before completing the three experimental sessions (two).

Procedures

All participants undertook three facial recognition tasks and an emotion prosody task on three separate occasions. Individuals rated their mood at the time of testing on a 10 cm scale ranging from ‘most depressed ever’ on the extreme left (scoring 0) to ‘most happy ever’ on the right (scoring 100). The midpoint was not indicated on the scale (Reference DavidDavid, 1989).

Analyses

The emotion items were grouped into two valence categories. Happiness (enjoyment), interest and surprise were categorised as ‘positive’ and sadness (distress), anger, fear, shame, contempt and disgust as ‘negative’ for both facial and vocal stimuli (Reference IzardIzard, 1971). The mean recognition accuracy (percentage correct) was computed for each valence category for each stimulus type for each group of participants. A repeated-measures analysis of variance (ANOVA) was employed to determine the main effects of group, emotion category and individual emotion, and interactions between these factors, on both facial and vocal tasks. Post hoc Tukey tests were then employed to examine specific differences in performance between groups. The influence of independent variables (e.g. age, education and current mood) on the performance of the perception tasks was controlled via analyses of covariance (ANCOVAs). Finally, Pearson correlations were performed between mean accuracy scores and clinical variables (e.g. PANSS score, neuroleptic dose, number of admissions).

Clinical and demographic data

Patients in the early stages of schizophrenia were significantly younger than healthy controls (P<0.001); there was no significant age difference between patients with chronic schizophrenia and healthy controls (P=0.90). Furthermore, healthy controls had more years of education than patients in the early stages of illness (P<0.05); other group comparisons were not statistically significant (Table 1).

Benton Facial Recognition Test

Analysis of variance revealed a main effect of group on performance on this task (F=16.85; d.f.=2,147; P<0.001). Patients in later stages of schizophrenia were less accurate than those in the early stages of illness (mean difference=4.63; P<0.05) and healthy controls (mean difference=10.18; P<0.001); patients in the early stages of schizophrenia were more impaired than healthy controls (mean difference=5.55; P<0.01; Table 1).

Analysis of covariance (mean score as dependent variable) were carried out with age, education and current mood as covariates. The effect of group upon performance on this test remained highly significant (F=16.17; d.f.=2,15; P<0.001) after controlling for these covariates. Years of education, current mood, severity of illness, neuroleptic dose, duration of illness and number of prior admissions did not correlate significantly with mean BFRT score in patients. Performance of males and females did not differ significantly on this test in any of the groups.

Facial Emotion Recognition Test

The effect of group

A significant main effect of group was found for performance on the FERT (F=51.34; d.f.=2,147; P<0.001). Patients in later stages of schizophrenia demonstrated a significantly greater impairment in their recognition of facial emotions compared with those in the early stages of illness (mean difference=8.33; P<0.001) and healthy controls (mean difference=21.74; P<0.001). A significantly greater impairment was found in patients in the early stages of schizophrenia compared with healthy controls (mean difference=13.41; P<0.001; Table 2).

Table 2

Facial expression recognition accuracy for the three groups

Stimuli	Healthy controls (% correct)	Patients in early stages of schizophrenia (% correct)1	Patients with chronic schizophrenia (% correct)1	F
Interest	70.5 (21.2)	60.0 (22.0)*†††	41.5 (23.4)***	21.7
Happiness	100.0 (0.0)	90.0 (14.9)**	90.5 (5.8)***	9.0
Surprise	87.5 (19.1)	72.50 (17.6)**	68.0 (23.1)***	12.8
Sadness	89.0 (12.5)	75.5 (17.8)***	72.5 (22.1)***	11.9
Disgust	65.0 (27.7)	51.5 (22.25)*†	39.5 (24.7)***	13.0
Contempt	51.5 (26.9)	37.5 (25.8)*	32.50 (27.3)**	6.8
Anger	93.5 (12.2)	88.5 (16.1)†	78.5 (23.6)***	9.0
Shame	55.0 (24.7)	37.0 (22.7)***†	26.5 (17.8)***	21.5
Fear	91.5 (15.6)	76.5 (22.81)**††	63.0 (28.2)***	19.5
Positive emotions	86.1 (10.6)	74.5 (13.2)***††	66.6 (15.0)***	27.6
Negative emotions	74.3 (11.9)	61.1 (11.8)***††	52.0 (14.0)***	38.9
Total	79.1 (8.9)	65.6 (9.7)***†††	57.3 (13.1)***	51.3

Voice Emotion Recognition Test

Effect of group

One-way ANOVA revealed a main effect of group (F=108.77; d.f.=2,147; P<0.001) on the total performance on the VERT.

Patients with chronic schizophrenia were significantly more impaired than patients in the early stages of illness (mean difference=12.62; P<0.001), and both patient groups were significantly more impaired than healthy controls (mean difference>27.94; P<0.001 for both comparisons) on this task (Table 3; Fig. 1).

Fig. 1.

Facial and vocal emotion recognition (% correct) in healthy controls (▪), patients in early stages of schizophrenia (▒) and patients in late stages of illness (□).

Table 3

Prosody recognition accuracy for the three groups

Stimuli	Healthy controls (% correct)	Patients in early stages of schizophrenia (% correct)1	Patients with chronic schizophrenia (% correct)1	F
Happiness	92.9 (11.3)	70.4 (21.8)***†	59.6 (24.0)***	36.3
Sadness	85.0 (16.7)	48.4 (28.5)***†	36.0 (16.1)***	56.1
Fear	84.2 (17.9)	50.0 (31.1)***	44.0 (31.2)***	29.7
Anger	97.1 (7.1)	71.2 (21.0)***†††	54.8 (30.4)***	48.3
Surprise	84.6 (11.8)	70.4 (21.4)**†	58.8 (28.4)***	16.9
Disgust	72.5 (24.3)	31.6 (23.9)***†	17.9 (22.3)***	68.9
Neutral	94.2 (11.9)	79.2 (23.8)**†	66.8 (26.3)***	20.1
Positive expressions	88.7 (8.1)	70.4 (17.1)***††	59.2 (22.9)***	36.7
Negative expressions	84.7 (11.8)	50.3 (16.2)***†††	38.1 (17.2)***	122.3
Total	86.9 (9.2)	58.6 (14.7)***†††	46.1 (17.0)***	108.7

Cross-modal emotion recognition impairment

First, all patients with schizophrenia were impaired in the recognition of emotional and non-emotional facial and vocal stimuli, supporting findings from previous studies demonstrating a generalised perceptual deficit in schizophrenia (Reference Kerr and NealeKerr & Neale, 1993; Reference Mandal, Pandey and PrasadMandal et al, 1998; Reference Hooker and ParkHooker & Park, 2002). The deficit in emotion recognition in all patients with schizophrenia remained significant even after covarying for the impairment in non-emotional face and voice recognition, supporting previous data indicating a specific deficit in emotion identification in schizophrenia (Reference Silver, Shlomo and TurnerSilver et al, 2002). The presence of deficits in more than one sensory modality (Reference Kee, Kern and MarshallKee et al, 1998; Reference Edwards, Pattison and JacksonEdwards et al, 2001; Reference Hooker and ParkHooker & Park, 2002) suggests a cross-modal emotion processing deficit. The right hemisphere has been linked with face and emotion processing (Reference BorodBorod, 2000). Our findings may therefore suggest a role for right hemisphere dysfunction in schizophrenia.

Interestingly, there were only small positive correlations between the magnitude of the overall deficits in emotion recognition for stimuli of each sensory modality in both healthy controls and patients. These were not present for individual emotions in either group, however. It is therefore possible that different emotions are displayed and recognised more easily in different sensory modalities, e.g. happiness may be recognised more easily from a face than a voice.

Impairments in positive and negative emotion recognition

Second, patients with schizophrenia demonstrated marked impairments overall in the recognition of negative and positive emotions, consistent with some (Reference Schneider, Gur and GurSchneider et al, 1995) but not all previous findings (Reference Mandal, Pandey and PrasadMandal et al, 1998; Reference BorodBorod, 2000). We also examined the ability of patients with schizophrenia to identify individual emotions. Overall, all patients were significantly less accurate than healthy volunteers in recognising all emotional stimuli, but were relatively less impaired in the identification of happiness, particularly from faces. Others have also demonstrated greater accuracy in the recognition of happiness than negative emotions by patients with schizophrenia (Reference Dougherty, Bartlett and IzardDougherty et al, 1974), and a relatively greater impairment in the identification of negative compared with positive emotional stimuli in these patients in facial (Reference Mandal, Pandey and PrasadMandal et al, 1998) and non-visual modalities (Reference BorodBorod, 2000; Reference Edwards, Pattison and JacksonEdwards et al, 2001).

Greater impairment in later stages of illness

Third, our findings also demonstrated that patients in later stages of schizophrenia were significantly impaired compared with those in the early stages of illness and healthy controls (Reference Silver, Shlomo and TurnerSilver et al, 2002) in recognising all examined expressions. This suggests a progressive impairment in emotion identification in schizophrenia, which may have resulted from treatment with typical antipsychotics, institutionalisation or the illness itself. We concede, however, that only a prospective design would allow us to determine whether emotion perception deficits were truly progressive in schizophrenia. An alternative explanation is that individuals in later stages of illness represented a distinct subgroup of patients, and would support the presence of heterogeneity within schizophrenia rather than illness progression. These two possibilities are not mutually exclusive, however.

No correlation between symptom severity and emotion recognition deficits

Finally, we did not demonstrate significant correlations between performance on any of the emotion recognition tasks and the examined clinical variables. This might be explained by some recent models that advocate progressive, essentially neurodegenerative processes involving excitotoxicity in addition to neurodevelopmental processes (Reference Garver, Nair and ChristensenGarver et al, 1999). Here, illness duration rather than symptom ratings would then be predicted to be correlated with task performance deficits. We did not, however, demonstrate such a correlation either; rather we merely demonstrated that individuals in the later stages of illness were more impaired than those in earlier stages.

Deficits in emotion recognition and social dysfunction

We have provided evidence for the presence of pervasive deficits in emotion recognition in more than one sensory modality in schizophrenia, which appears to increase with illness chronicity. These deficits are not specifically related to positive or negative symptoms, medication or current mood state. Our results are some of the first to suggest that in schizophrenia there might be progressive emotion processing deficits, which appear to be unrelated to specific symptom profiles but may be responsible for the social dysfunction observed in people with this disorder.

CLINICAL IMPLICATIONS

1. ▪ Assessment of the magnitude of emotion perceptual deficits in facial and vocal modalities in schizophrenia can be employed as a measure of illness progression.

2. ▪ These tests can be employed to examine the extent of heterogeneity within schizophrenia.

3. ▪ Future study should examine the extent to which training in emotion perceptual tasks improves illness outcome in schizophrenia.

LIMITATIONS

1. ▪ We employed static rather than dynamic facial expressions; the latter are more ecologically valid.

2. ▪ We employed a cross-sectional comparison rather than a longitudinal, prospective design. The latter would more readily determine the extent to which the emotion processing deficits in schizophrenia were progressive.

3. ▪ We were unable to assess in detail the potential effect of the type of antipsychotic treatment (atypical v. typical) on task performance.