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Open Access Highly Accessed Research article

Automatic amygdala response to facial expression in schizophrenia: initial hyperresponsivity followed by hyporesponsivity

Thomas Suslow12*, Christian Lindner1, Udo Dannlowski13, Kirsten Walhöfer1, Maike Rödiger1, Birgit Maisch4, Jochen Bauer1, Patricia Ohrmann1, Rebekka Lencer1, Pienie Zwitserlood5, Anette Kersting2, Walter Heindel6, Volker Arolt1 and Harald Kugel6

Author Affiliations

1 Department of Psychiatry, University of Münster, Albert-Schweitzer-Str. 11, Münster 48149, Germany

2 Department of Psychosomatic Medicine, University of Leipzig, Semmelweisstr 10, Leipzig 04103, Germany

3 Department of Psychiatry, University of Marburg, Rudolf-Bultmann-Str. 8, Marburg 35037, Germany

4 Klinik am Schlossgarten, Am Schlossgarten 10, Dülmen 48249, Germany

5 Department of Psychology, University of Münster, Fliednerstr. 21, Münster 48149, Germany

6 Department of Clinical Radiology, University of Münster, Albert-Schweitzer-Campus 1, Münster 48149, Germany

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BMC Neuroscience 2013, 14:140  doi:10.1186/1471-2202-14-140

Published: 13 November 2013

Abstract

Background

It is well established that the amygdala is crucially involved in the processing of facial emotions. In schizophrenia patients, a number of neuroimaging findings suggest hypoactivation of the amygdala in response to facial emotion, while others indicate normal or enhanced recruitment of this region. Some of this variability may be related to the baseline condition used and the length of the experiment. There is evidence that schizophrenia patients display increased activation of the amygdala to neutral faces and that this is predominantly observed during early parts of the experiment. Recent research examining the automatic processing of facial emotion has also reported amygdala hyperactivation in schizophrenia. In the present study, we focused on the time-course of amygdala activation during the automatic processing of emotional facial expression. We hypothesized that in comparison to healthy subjects, patients would initially show hyperresponsivity of the amygdala to masked emotional and neutral faces. In addition, we expected amygdala deactivation in response to masked facial emotions from the first to the second phase to be more pronounced in patients than in controls.

Results

Amygdala activation in response to angry, happy, neutral, and no facial expression (presented for 33 ms) was measured by functional magnetic resonance imaging in 30 schizophrenia patients and 35 healthy controls. Across all subjects, the bilateral amygdala response to faces (relative to the no facial expression condition) was larger in the initial phase (first half of trials) than in the second phase (second half of trials). During the initial phase, schizophrenia patients exhibited an increased right amygdala response to all faces and an increased left amygdala response to neutral faces compared with controls. During the second phase, controls manifested a higher right amygdala response for all faces and a higher left amygdala response to angry faces than patients.

Conclusions

Schizophrenia patients are characterized by high initial amygdala responsivity to facial expressions at an automatic processing level, which substantially decreases with time. Amygdala deactivation over time might reflect an automatic mechanism by which schizophrenia patients suppress the processing of facial stimuli. This blocking mechanism could help patients avoid overstimulation during social interactions.

Keywords:
Schizophrenia; Automatic processing; fMRI; Amygdala; Facial expression; Temporal dynamics