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Keywords:

  • event-related potentials;
  • facial affect;
  • P300;
  • paranoid type;
  • recovery period;
  • schizophrenia

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

Abstract The auditory P300 is affected by arousal and emotion. We examined the effect of drawings expressing sadness or pleasure on auditory event-related potentials (ERP) during recovery from schizophrenia. Oddball-paradigm auditory ERP were recorded while presenting one of these drawings to nine patients with paranoid schizophrenia and seven patients with other types of schizophrenia during the acute stage and again during remission. P300 parameters (amplitude, area, and latency), reaction time, and symptom scores were evaluated. P300 amplitude and area were significantly greater in the recovery than in the acute phase. Increases were larger when viewing drawings that expressed sadness than when viewing drawings that expressed pleasure. In paranoid-type patients, P300 when viewing pleasurable drawings was similar to that when viewing sad drawings during the acute phase; in remission, P300 was significantly larger when viewing sad drawings than when viewing pleasurable drawings. In non-paranoid patients, P300 while viewing pleasurable drawings was significantly larger than that while viewing sad drawings during the acute phase; this difference disappeared during recovery. P300 latency and reaction time were not influenced by facial-affect stimuli or recovery. A significant negative correlation was noted between amplitude and negative symptom scores. P300 amplitude and area may be useful state markers during recovery in schizophrenic patients. Effects involving attention resources and emotional arousal are also involved.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

Event-related potentials (ERP) have been studied as a practical biologic marker to investigate information processing in the human central nervous system.1–3 Amplitude of ERP varies widely depending on the complexity of the task, the level of arousal, and the emotional state. In studies of information processing in schizophrenic patients, the amplitude of the P300 component of ERP has been found to be attenuated.4 However, the few reports that have concerned the effects of facial-affect recognition on ERP have been limited to healthy subjects.5–7

Failure of emotional recognition has been advocated as a fundamental feature of schizophrenia, specifically reading emotion from a facial expression of anger, fear, joy, sorrow, displeasure, surprise, or shame.8–10 Particularly, impaired recognition of negative feelings, such as anger or fear may be prominent in schizophrenic patients, at least during the acute phase.10

Duncan et al. reported that visual P300 amplitude and area changed with recovery from the acute phase schizophrenic patients.11 Maeda et al. also found that auditory P300 amplitude and area significantly increased during remission in schizophrenic patients tested under the eyes-open condition.12 These findings indicate that visual information may be important in the remission process in schizophrenic patients. The present study was performed to examine the effect of visually presenting facial affect (sadness vs pleasure) on auditory P300 components in patients with schizophrenia.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

Subjects

We studied 16 schizophrenic patients (nine with paranoid type and seven with other types). Patients were diagnosed by two psychiatrists using DSM-IV. Patient ages ranged from 16 to 40 years (mean ± SD, 32.6 ± 6.1 for paranoid-type patients and 23.5 ± 7.5 for others). There was a significant age difference between paranoid type and non-paranoid patients. All patients were right-handed and all were medicated. Written informed consent was obtained from all patients prior to study.

Event-related potential recording

Event-related potentials were recorded from scalp electrodes placed at Fz, Cz, Pz, Oz, C3, and C4 according to the International 10–20 System referred to linked mastoids. Electroded were affixed above and below the right eye to monitor vertical eye movements. All impedances were kept below 5 KΩ and the bandpass filter was 0.16–120 Hz.13 Tone frequency was 2 kHz for target stimuli (probability 20%) and 1 kHz (probability 80%) for non-target stimuli presented at an appropriate intensity (sound presence level 60 dBSPL). Patients were asked to look closely at one of two simple drawings (one of pleasure or one of sadness) to evaluate the emotional facial expression.14 The largest differences in P300 amplitude and area were obtained between pleasure and sadness in healthy subjects and stable schizophrenic patients.15 Thus, in the present study, we used illustrated pleasant and sad facial pictures and did not use photographs. The averaged waveform was obtained 20 single artifact-free samples for one block at testing. Trials with amplitude exceeding 100 μV were rejected automatically from the averaging process. P300 peak amplitude was calculated from the baseline to the peak of the positive waveform within the time window of 250 to 500 msec. The averaged during 100 msec before stimulus was used as a baseline. It has been reported that the amplitude of P300 at Pz is largest using auditory oddball task.3 Thus, the differences were evaluated at the Pz site.

Event-related potential protocol

Event-related potentials were recorded at 14.00 and 16.00 h in two blocks (pleasure and sadness) using double tasks (counting and pressing a button upon hearing the target tone).12 The two drawings were shown to all patients in a counterbalanced manner. Event-related potentials were recorded in each subject in sessions during the acute phase (within 2 weeks of admission) and during remission (time of hospital discharge: 77.6 ± 26.5 days from admission).

Clinical evaluation and medication

Positive and negative symptom scores (PANSS)16 were evaluated at the time of ERP recording by two psychiatrists not measuring ERP. All patients were treated with neuroleptics; their mean dose in chlorpromazine equivalents was 411.4 ± 74.4 mg/day for non-paranoid patients and 448.9 ± 82.1 mg/day for paranoid type patients at the acute phase. There were no significant differences in doses between non-paranoid and paranoid type patients or between the acute phase and remission. All patients were treated with biperiden (4.0 ± 1.3 mg/day for non-paranoid patients and 3.8 ± 1.0 mg/day for paranoid patients).

Statistical analysis

For data considered reliable (epsilon < 1.0), only a two-way (session × electrode) repeated ANOVA was used. A three-way analysis of variance (ANOVA, session × emotion × electrode) was assessed for main effect. Fisher's protected least significant deviation (PLSD) was performed post-hoc for significant difference related to presented pictures and session of disease. Furthermore, three-way ANOVA (session × emotion × electrode) for each subtype and one-way ANOVA (session) involving each electrode and emotion also were evaluated. Relationships between variables were assessed using Pearson's correlation coefficients. A probability lower than 5% was considered significant.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

The P300 component

Amplitude

In a three-way ANOVA (session × emotion × electrode) with session as the main effect, the amplitude significantly increased in remission beyond that seen in the acute phase (F1,360 = 58.7, P < 0.0001). No significant difference was observed between sadness and pleasure conditions with emotion as the main effect. However, at the Pz lead, a significant increase in amplitude was obtained while viewing sadness (P < 0.001) but not pleasure as shown in Figs 1 and 2.

image

Figure 1. Changes of P300 amplitude when viewing sadness. Left: averaged wave form at each electrode site (––, acute phase; —, recovery phase). Note that P300 amplitude clearly increased at recovery phase in all electrode sites. Right: P300 amplitude in ordinate was plotted against electrode site in abscissa. The each bar represents the mean ± SEM of amplitude. P < 0.05; ★★P < 0.01; ★★★P < 0.001.

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image

Figure 2. Changes of P300 amplitude while viewing pleasure. Left: averaged wave form at each electrode (––, acute phase; —, recovery phase). Right: P300 amplitude (ordinate) as a function of lead (abscissa). The each bar represents the mean ± SEM of amplitude.

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In paranoid-type patients, significant increases were obtained for session (F1,192 = 60.5, P < 0.001) and for expression (F1,192 = 5.0, P < 0.05) as shown in Figure 3. At the Pz lead, a significant increase in amplitude was obtained (P < 0.01). In non-paranoid patients, significant increases were obtained for session (F1,192 = 9.5, P < 0.01) but not for expression (F1,192 = 2.0, P = 0.16) as shown in Figure 3. At the Pz lead, a significant increase in amplitude was obtained (P < 0.05).

image

Figure 3. P300 amplitude for non-paranoid patients (left) and paranoid type patients (right). Left: P300 amplitude (ordinate) as a function of lead (abscissa) (○, acute phase; □, recovery phase). Right: P300 amplitude (ordinate) as a function of lead (abscissa) (▵, acute phase; ◊, recovery phase). Note that P300 amplitude increased significantly at all electrodes in paranoid type patients. P < 0.05; ★★P < 0.01; ★★★P < 0.001.

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Area

Area significantly increased in the remission phase (F1,360 = 38.3, P < 0.0001) using a three-way ANOVA with the main effect being session. There was no significant difference observed between viewing sadness and pleasure. However, at the Pz lead, a significant increase in area was obtained viewing sadness (P < 0.01), not pleasure. In paranoid-type patients, significant differences were obtained for session (F1,192 = 49.7, P < 0.0001) and for expression (F1,192 = 4.4, P < 0.05). The area while viewing sadness was significantly larger than that while viewing pleasure. At the Pz lead, a significant increase in area was obtained (P < 0.05). In non-paranoid patients, significant increases were obtained for session (F1,192 = 4.1, P < 0.05) but not for expression. At the Pz lead, no significant increases in area were obtained.

Latency

No significant difference was seen for session (F1,360 = 0.3, P = 0.57) or emotion (F1,360 = 2.5, P = 0.11) using a three-way ANOVA. In paranoid-type patients, there was significant main effect seen for session or emotion. In non-paranoid patients, a significant main effect was seen for emotion; the latency when viewing pleasure was significantly shorter than that with sadness (F1,144 = 6.5, P < 0.05).

Reaction time

There were no significant differences obtained using a three-way ANOVA (session × emotion × subtype).

Accuracy of counting and button pressing

There were no significant differences obtained using a three-way ANOVA (session × emotion × subtype).

Symptom scores and drugs

Negative symptom scores showed a significant negative correlation with amplitude (r = − 0.52, P < 0.001) and area (r = − 0.53, P < 0.001). While sadness, the correlation coefficient with amplitude (r = − 0.65, P < 0.001) was larger than that with pleasure (r = − 0.41, P < 0.05). These effects were not seen with positive symptom scores. There were no significant relationship noted between the dose in chlorpromazine equivalents and P300 parameters.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

P300 components as state markers

Many reports have characterized P300 amplitude attenuation in schizophrenic patients as a trait marker.4 Duncan et al. concluded that only visual P300 showed state dependence, improving with clinical recovery.11 However, Maeda et al. reported that the auditory P300 component (amplitude and area) also increased with recovery but only in examinations conducted with eyes open.12 This indicated that visual information is important in the difference related to recovery. In the present study, both P300 amplitude and area significantly increased with the improvement of illness. Furthermore, these P300 measures showed significant negative correlation with negative symptom scores. These results suggested that such P300 measures as peak amplitude and area may be markers for the pathologic state as reported previously.11,12 Notably, improvement of these P300 values were most marked for the sad emotion and were less prominant for the pleasant emotion. The difference was not significant for P300 latency, suggesting that the changes in P300 involved allocation of attention resources as advocated by Polich,3 rather than speed of attention resource allocation. Interestingly, improvements in P300 parameters were observed for all electrode sites in paranoid type patients, but only at the Pz site in non-paranoid patients. These indicate that some spatial differences exist in the distribution of cognitive information processing between paranoid and non-paranoid patients, as reported in the situation of facial emotion recognition.17

Effect of facial affect recognition on the P300 component

Schizophrenic patients manifest a significant deficit in identifying emotion in facial expressions.10 Lewis and Garver reported that impairments in facial-affect recognition were relatively stable in individual patients and that such deficits were related to negative symptoms; that diagnostic subtype, therefore, would be related to deficient ability to recognize affect.17 However, there is no study concerning the effect of facial affect upon P300 components in schizophrenic patients. Recently, Yamaguchi et al. demonstrated an effect on auditory P300 components from simple visual emotional stimulation (faces showing sadness, pleasure, anger or neutrality) that might influence emotions in stabilized schizophrenic patients differently than that in healthy subjects.15

The visual competition for attention resources inducing the auditory P300 that took place in healthy subjects, was not seen in schizophrenic patients, reflecting a failure of expression recognition in schizophrenic patients. Lang et al. examined visual ERP in healthy subjects, reporting that P300 amplitude for a face showing anger was significantly larger than for laugh indicating an increase in attention.6 Greater amplitude with an angry face may indicate that subjects were more engaged by an angry expression than by a happy one, or it could mean that the visual configuration itself was more complex with the angry face than with that expressing pleasure.6

In the present study, there was no significant difference in the P300 amplitude among patients, suggesting that schizophrenic subjects showed a defect in identifying emotion in facial expressions. However, a significant difference was noted between sadness and pleasure in paranoid-type patients. Both amplitude and area were greater when viewing sadness than when viewing pleasure. However, relatively little difference was observed in non-paranoid patients. These findings are consistent with observations that paranoid patients recognize facial expression better than non-paranoid patients.17,18 Significant differences in P300 amplitude and area were observed only in remission in the paranoid-type patients; values when viewing sadness were larger than values when viewing pleasure. These suggest that the attention of the subject increases when viewing sadness and that subjects were more engaged by sad expression than by one expressing pleasure, similar to healthy subjects.15 These results suggested that facial-affect recognition is deficient in schizophrenic patients but may improve with recovery, especially in paranoid-type patients.

Human facial-affect recognition triggers a mental process. The emotion is recognized, the context is evaluated and appropriate action is taken. We hypothesize that in the acute phase of illness, schizophrenic patients may respond by identifying emotionally with a sad face presented to them, but tend to pay less attention to the task as a result. Later, cognitive feedback may recover to better deal with the negative emotional load of a sad face presented in convalescence. The effects from an angry face may be similar.6

The correlation coefficient between P300 amplitude or area and negative symptom scores was larger for sadness (negative affect) than for pleasure (positive affect); the ability to feel sadness was clearly state-dependent.17 The absence of latency effects from the facial-affect stimuli suggest that stimulus evaluation time was similar for the pair of faces; subjects found the faces equally discriminable. Significant changes in P300 parameters with facial-affect recognition, then seem to involve attention resources, as Polich argued.3

Finally, auditory P300 assessed with a negative emotional stimulus might be used as a marker in schizophrenic patients. However, it is noted that the facial emotional expression study cannot be applied to a psychiatric setting without first refining it for cultual differences.14 Further study as to how changes influence visual stimuli on the recovery of P300 component should be undertaken. Failure to accurately read non-verbal cues indicating emotion may contribute to patients' inappropriate social responses, as well as decrease their sense of social effectiveness. Improving social skills of schizophrenic patients might benefit from focusing on training in emotion perception.

ACKNOWLEDGMENT

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES

This work was supported by grant number 11670971 (1999) from Japanese Grant-In-Aid for Scientific Research.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENT
  8. REFERENCES
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