Multisensory integration of emotionally valenced olfactory-visual information in patients with schizophrenia and healthy controls

Abstract

Background: Patients with schizophrenia frequently have deficits in social cognition, and difficulties in the discrimination of emotional facial expressions have been discussed as an important contributing factor. We investigated whether this impairment is aggravated by difficulties relating the observed facial expression to contextual information, as is often provided by emotionally valenced crossmodal stimulation.

Methods: We investigated the effects of odorant primes on the accuracy and speed of emotional face recognition. Healthy controls and patients with schizophrenia were exposed to 2-second odorant stimuli: vanillin (pleasant), ambient air (neutral) and hydrogen sulfide (unpleasant). The odours were followed by an emotional face recognition task, in which participants determined if a face showed happiness, disgust or neutral affect.

Results: Controls showed improved performance in the categorization of disgusted faces after all types of odour stimulation irrespective of the emotional valence. However, in controls, the response time for happy faces was slower after presentation of any odour. Schizophrenia patients showed an attenuated effect of olfactory priming on disgust recognition, which resulted in the increased performance differences between the groups. This effect was particularly strong for the unpleasant odour.

Limitations: The study design did not allow us to fully differentiate between the effects of perceived odour intensity and valence. A possible contribution of cognitive deficits on the observed effects should be investigated in future studies.

Conclusion: Our results provide novel evidence for a special connection between the presentation of odorant cues and the accuracy of recognition of disgusted faces in healthy controls. This recognition advantage is disturbed in patients with schizophrenia and appears to contribute to the observed deficit in emotional face recognition.

Fig. 1

Illustration of the experimental procedure. Three consecutive trials are shown (incongruent–unpleasant odour, congruent–neutral odour, incongruent–pleasant odour). During each trial, participants were presented with an odorant airpuff followed by a picture of an emotional face. The odours were vanillin, hydrogen sulfide or ambient air, and the faces showed happiness, disgust or no emotion. Participants were asked to determine the emotional expression of the face. The responses were recorded during face presentation, and visual feedback was provided. The interstiumulus interval (ISI) between trials was 1000 ms.

Fig. 2

Mean intensity (A) and pleasantness (B) ratings for vanillin, ambient air and hydrogen sulfide (H₂S). Ratings were converted from the Self-Assessment Manikin rating scales filled out by the participants after completion of the task. Error bars indicate +/− 1 standard error. The p values show significant within-group differences.

Fig. 3

Accuracy of emotion recognition among healthy participants and schizophrenia patients. We excluded nonresponses. The x-axis indicates the condition separately by odour and emotional face presented. Error bars indicate +/− 1 standard error. The p values show significant group differences between controls and patients.

Fig. 4

Log-transformed reaction times to the facial emotion recognition task (correct trials only). The left graph shows results for controls, the right graph shows results for patients. The x-axis indicates the condition separately by odour and emotional face presented. Error bars depict +/− 1 standard error.