Elsevier

Biological Psychiatry

Volume 53, Issue 12, 15 June 2003, Pages 1099-1112
Biological Psychiatry

Original article
Right lateral fusiform gyrus dysfunction during facial information processing in schizophrenia

https://doi.org/10.1016/S0006-3223(02)01784-5Get rights and content

Abstract

Background

Patients with schizophrenia exhibit facial information processing deficits that likely contribute to their social dysfunction. Whether the deficits involve facial affect and/or identity processing or result from other cognitive abnormalities in schizophrenia remains controversial, and a brain dysfunction specifically related to them has never been reported. If such dysfunction existed, it should be consistently observed across groups of patients and during performance of different facial information processing tasks, independently of whether such tasks demand working memory (WM), semantic, or other cognitive processes. We hypothesized that the right lateral fusiform gyrus (rLFG), one of several human brain areas involved in facial information processing, would consistently show activation abnormalities during both facial affect and identity discrimination in schizophrenia.

Methods

We used functional magnetic resonance imaging to measure brain activation in two groups of six chronic, stable schizophrenic outpatients and two of six age- and gender-matched healthy controls. One group of patients and one of controls performed facial affect—with or without semantic processing—and identity discrimination tasks, and the other two groups WM tasks with facial expression cues and varying attentional demands.

Results

Patients from either group failed to activate the rLFG when compared to controls in any task. Other activation abnormalities were task-specific (i.e., seen only during performance of one set of tasks) and not consistently observed in both groups of patients, and thus could not be directly and solely linked to facial information discrimination.

Conclusions

These results indicate a specific rLFG dysfunction during early facial information—identity or affect—processing, independent from other cognitive deficits, in schizophrenia.

Introduction

Information conveyed by human faces is crucial for social interaction, adaptation, and functioning. In normal individuals, several brain areas are in one way or another involved in finely discriminating and interpreting that information so that it can be used as cues for our social decision making Adolphs 1999, Adolphs et al 1996, Allison et al 2000, Bruce and Young 1986, Haxby et al 1996, Haxby et al 2000. The posterior aspects of the superior temporal sulcus (STS) and the amygdala, for example, have been respectively implicated in the perception of motion-related and emotional/social features of that information Brothers 1995, Bruce and Young 1986, among several other roles. The anterior cingulate cortex (ACGC), the inferior (IFC), the orbito-frontal (OFC), and the posterior parietal (PPC) cortex exhibit activations during performance of facial information processing tasks with different cognitive demands Alexander et al 1999, Dolan et al 1996, Haxby et al 1996, Maguire et al 2001. But one area in particular, the lateral fusiform gyrus (LFG)—especially in the right hemisphere—seems to be highly specialized in finely discriminating and processing invariant aspects of human face information Adolphs et al 1996, Allison et al 2000, Dolan et al 1996, Haxby et al 2000, Kanwisher et al 1997, Kim et al 1999, Maguire et al 2001, Nakamura et al 2000, Puce et al 1995, Rossion et al 2000, Sams et al 1997. This area becomes more specifically activated when subjects attend to pictures of human faces than when they attend to other complex objects, including scrambled composites of similar pictures Allison et al 1994, Kanwisher et al 1997, Kim et al 1999, Maguire et al 2001, Nakamura et al 2000, Puce et al 1995, Rossion et al 2000. Lesions of the right temporo-parietal junction (Bowers et al 1985), which plays an important role in processing emotions conveyed by facial expressions Adolphs et al 1996, Gur et al 1994, generally involve the right LFG or affect its function by altering its connectivity and result in impairments in recognizing facial expressions Bowers et al 1985, De Renzi 1997. The right LFG has also been termed fusiform face area(Kanwisher et al 1997).

It has been known for more than 40 years that subjects with schizophrenia have difficulties processing (i.e., discriminating, interpreting) facial information Addington and Addington 1998, Borod et al 1993, Dougherty et al 1974, Habel et al 2000, Muzekari and Bates 1977, Streit et al 1997; reviewed in Hellewell and Whittaker 1998). The results of multiple studies confirming such findings do not offer clues about what neural dysfunctions, if any in particular, might explain those deficits. Furthermore, schizophrenic subjects also exhibit a variety of cognitive deficits in attention, concentration, working memory (WM), and semantic processing Bellack et al 1989, Jeste et al 1996, Mueser and Tarrier 1998. There is no agreement about whether facial information processing abnormalities in schizophrenia result from these deficits or are the direct consequence of specific, separate cerebral dysfunctions that may impact processing of facial information in general or facial affect in particular Archer et al 1992, Archer et al 1994, Blanchard and Neale 1994, Cutting 1981, Dougherty et al 1974, Feinberg et al 1986, Frith et al 1983, Gessler et al 1989, Heimberg et al 1992, Kerr and Neale 1993, Novic et al 1984, Penn et al 2000, Pollard et al 1995, Walker et al 1984 in the condition. Only a couple of recent studies have addressed issues related to the goal of the present study. One of them (Quintana et al 2001) reported abnormally increased cortical activity—likely compensatory—during WM processing of simple emotional expressions (i.e., sadness, happiness) conveyed by facial diagrams in the motor and premotor areas—the mirror system for mouth and lips gestures—of schizophrenic subjects, who also exhibited concurrent activation deficits in the lateral OFC. These results suggest that basic facial information processing mechanisms might be abnormal in schizophrenia (Quintana et al 2001). The other study, using magnetoencephalography (Streit et al 2001), reported distributed, performance-related weakening of cortical activity in partly remitted schizophrenic patients while they were categorizing facial emotions. Evidence of abnormal brain function that may closely relate to deficits in facial information processing seen in schizophrenic subjects, or that may discern the specificity of these deficits, has not been previously reported.

We designed a study to test the hypothesis that there is a specific, separate brain dysfunction related to facial information (affect and identity) processing deficits in schizophrenia. Such a deficit should be repeatedly observed in different and nonoverlapping groups of patients and during the performance of a variety of tasks that require discrimination of facial affect or identity independently of demands on WM and other cognitive processes, including semantic ones. We also hypothesized that such a putative dysfunction would be observed in the early stages of facial information discrimination and that the right LFG would be the best candidate for showing it. To test our hypotheses, we used functional magnetic resonance imaging (fMRI), whose signal variations detect localized relative changes in blood flow, volume, and oxygenation (blood oxygen level dependent, BOLD) that have been shown to be a correlate of neuronal function Heeger and Ress 2002, Logothetis et al 2001.

Section snippets

Subjects

We recruited 12 schizophrenic patients (eight male, four female, mean age 31.25 ± 9.46 years) diagnosed according to DMS-IV criteria (American Psychiatric Association 1994) by at least two board-certified psychiatrists. We also recruited 12 healthy, normal volunteers (five male, seven females, mean age 26.82 ± 3.79 years) matched by age to their patient counterparts. All subjects were right-handed according to self-report and to responses to the items of a modified Edinburgh handedness

Performance

Logistic and multiple regression model analyses of, respectively, response accuracy levels and reaction times did not reveal any significant group (i.e., control subjects or patients) or group × task interaction effects on the data. Hence, in terms of response accuracy and reaction time, the overall task performance in both subject groups was statistically similar. These data analyses showed several traits that further establish that the patients indeed actively performed the tasks and attended

Discussion

The results reveal a consistent deficit in the function of the right LFG during performance of any of the facial information (identity or affect) processing tasks studied in all our schizophrenic patients. Given the limited number of subjects performing each task, our results cannot strictly be extrapolated to the general population of patients with schizophrenia. Neither can they be used to directly explain the deficits in social adjustment and functioning that those patients exhibit.

Acknowledgements

Supported by a Department of Veteran Affairs (Office of Research and Development, Medical Research Service) Advanced Research Scientist Career Development Award, and by a National Alliance for Research on Schizophrenia and Depression Staglin Young Investigator Award to JQ, as well as by contributions from the VA’s Veterans Integrated Service Network-22, Mental Illness Research Education, & Clinical Center, the Howard Hughes Medical Institute (Frontiers of Science, UCLA School of Medicine), the

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