Physiological responsivity to emotional pictures in schizophrenia

Abstract

Schizophrenic patients are known to experience difficulties in emotional information processing, yet knowledge of their physiological responsivity to emotional stimuli is limited. The purpose of this study was to investigate the physiological reactions of schizophrenic patients to emotional stimuli. We presented pictures selected from the International Affective Picture System (IAPS) to patients and controls, while assessing their subjective evaluations in terms of valence and arousal scores and measuring their responses of heart rate (HR), breathing rate (BR), skin conductance level (SCL) and diastolic (DBP) and systolic blood pressure (SBP). For the analysis of the physiological data, three emotional picture categories were formed: positive (erotic content), negative (physical injuries) and neutral (landscapes). Patients and controls did not differ in their subjective evaluations of the pictures. Also, for both patients and controls, the SCL and DBP responses to positive emotional pictures were larger as compared to negative and neutral pictures. However, the patients did show significantly increased HR responses to the positive emotional pictures as compared to controls, possibly as a result of a decreased parasympathetic activity. Only for the BR response to the positive emotional pictures did we observe significant positive correlations with the PANSS scores. These first data suggest that altered physiological responsivity to emotional pictures in schizophrenia is limited to those with positive emotional content. Further studies will need to refine the dynamics of this stimulus category in relation to clinical state and medication effects.

Introduction

Schizophrenia is a psychiatric illness which causes both emotional as well as cognitive disturbances (Bleuler, 1911, Kraepelin, 1919). Bleuler (1911) defined schizophrenia essentially as a splitting of thoughts from feelings. Blunted affect and anhedonia have been recognised as core features of the disorder since this first description (Philips et al., 2003). Abnormalities in emotion identification and emotional behaviour have also been found to be associated with the poor social functioning observed in patients with schizophrenia (Borod and Madigan, 2000).

Over the past decade the emotional disturbances schizophrenic patients experience have received increasing attention (Edwards et al., 2001). Schizophrenic patients appear to have an impairment in recognising faces and emotional facial expressions (Addington and Addington, 1998, Kohler et al., 2003), as well as an impairment in identifying affective prosody (Edwards et al., 2001). Baudouin et al. (2002) found that the emotion processing deficit schizophrenic patients experience was related to negative symptoms and that the inability to selectively attend to emotion was correlated with the severity of the negative symptoms, although Kohler et al. (2000) found a positive correlation between emotion recognition and both negative and positive symptomatology.

Although individuals with schizophrenia exhibit significantly diminished facial expressions of emotion, patients report an emotional experience that is equal to or possibly greater than that of non-psychiatric controls (Aghevli et al., 2003, Earnst and Kring, 1999). These findings of Aghevli et al. (2003) support the existence of a discrepancy between the expression and experience of emotion in schizophrenia which is consistent with the inhibition model of blunted affect as suggested by Bleuler (1911), in which patients with schizophrenia are assumed to experience a normal range of emotions but do not reflect this in their emotional expression. However, an emotional experience comprises not only its subjective expression in terms of language or expressed feelings, but also its underlying physiological concomitants. These last processes are less well studied in schizophrenia.

Lang et al. (1998) have postulated the existence of two motivational systems in the brain, i.e., appetitive (positive emotions) and defensive (negative emotions), that each can vary in terms of activation or arousal. Arousal here is not viewed as having a separate substrate, but rather as representing the intensity of activation of either the appetitive or the aversive system or the coactivation of both systems, which may be reflected in physiological processes. Although research investigating the emotional disturbances in schizophrenic patients has thus far mainly focused on the recognition of faces and facial expressions, it is also relevant to investigate the emotional disturbances that schizophrenic patients experience daily in their environment in relation to their physiological responsivity. For this purpose, pictures of affective events and objects can be used. Emotional pictures are ecologically valid stimuli in the sense that they involve processing of the kinds of visual material that people encounter frequently in their daily lives (Bradley and Lang, 1999). Furthermore, the validity of emotional pictures in investigating emotional processing and brain activity has been demonstrated by several neuroimaging studies in which pictures with emotional content, selected from the International Affective Picture System (IAPS; Center for the Study of Emotion and Attention, 1997), were presented to subjects (Hariri et al., 2002, Hariri et al., 2003, Moratti et al., 2004, Müller et al., 2003, Phan et al., 2004).

Lang et al. (1997) have developed the International Affective Picture System (IAPS; Center for the Study of Emotion and Attention, 1997), a set of over 600 pictures, which includes normative ratings of the levels of pleasure and arousal associated with each picture. In healthy subjects, pictures with scenes of threat, violent death and erotica cause the strongest subjective emotional arousal and the largest physiological responses such as reflected in skin conductance level (SCL), whereas, unrelated to subjective arousal, unpleasant-evaluated pictures induce a greater heart rate (HR) deceleration and pleasant pictures a relatively greater peak acceleration (Bradley and Lang, 2000). At present, there are no such data available from patients with schizophrenia.

Apart from subjective evaluations, physiological responses to emotional stimuli in schizophrenia may be influenced by pathophysiological factors associated with distinct symptom domains (Buchanan and Carpenter, 1994). For instance, physiological variables have been associated with the presence of both positive and negative symptoms. There has been a tendency for positive symptoms to be associated with an increased skin conductance orienting response (SCOR), but these findings have been very mixed (Dawson et al., 1989, Green et al., 1989, Gruzelier and Raine, 1994, Zahn et al., 1991). With respect to HR, only a few studies have attempted to link tonic and phasic HR to schizophrenic symptomatology (Brekke et al., 1995). Toichi et al. (1999) found that the presence of a psychotic state suppresses HR variability, whereas schizophrenic patients with negative symptoms and ventricular enlargement have been found to show reduced resting HR (Cannon et al., 1992). Brekke et al. (1995) showed that negative symptoms were related to deficits in visuomotor processing, lower resting HR and increased HR reactivity to stress. They also observed that disorganised symptoms were related to increased SCOR and lower skin conductance stress reactivity. Overall, these data underline the relevance to study physiological responsivity to emotional stimuli in relation to the clinical symptoms of the schizophrenic patients.

The purpose of this study was to investigate the physiological reactions of schizophrenic patients to pictures with emotional content. During the presentation of pictures selected from the IAPS (Center for the Study of Emotion and Attention, 1997), HR, SCL, breathing rate (BR), and diastolic and systolic blood pressure (DBP, SBP) were measured in order to identify alterations in responsivity to emotional stimuli of schizophrenic patients as compared to normal controls. Additionally, we assessed their subjective evaluations of the pictures in terms of valence and arousal ratings. Because scenes of threat, violent death and erotica cause the strongest emotional arousal and the largest physiological responses (Bradley et al., 2001), we focused on pictures depicting erotica (positive emotions), mutilations and burns (negative emotions), and landscapes (neutral). Furthermore, we investigated the relationship between clinical symptom severity and physiological responsivity in schizophrenic patients, using the Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987). By combining physiology with subjective evaluations and clinical symptoms, we hoped to increase our understanding of emotional disturbances in schizophrenic patients.