Neural circuitry of emotional face processing in autism spectrum disorders

Neural circuitry of emotional face processing in autism spectrum disorders

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J Psychiatry Neurosci 2010;35(2):105-114

Christopher S. Monk, PhD; Shih-Jen Weng, PhD; Jillian Lee Wiggins, MS; Nikhil Kurapati, BS; Hugo M.C. Louro, MSE; Melisa Carrasco, MS; Julie Maslowsky, MA; Susan Risi, PhD; Catherine Lord, PhD

Monk, Weng, Wiggins, Kurapati, Louro, Maslowsky, Lord — Department of Psychology; Monk, Lord — Center for Human Growth and Development and Department of Psychiatry; Monk, Carrasco — The Neuroscience Program, University of Michigan; Risi, Lord — University of Michigan Autism and Communications Disorders Center, Ann Arbor, Mich.

Abstract

Background: Autism spectrum disorders (ASD) are associated with severe impairments in social functioning. Because faces provide nonverbal cues that support social interactions, many studies of ASD have examined neural structures that process faces, including the amygdala, ventromedial prefrontal cortex and superior and middle temporal gyri. However, increases or decreases in activation are often contingent on the cognitive task. Specifically, the cognitive domain of attention influences group differences in brain activation. We investigated brain function abnormalities in participants with ASD using a task that monitored attention bias to emotional faces.

Methods: Twenty-four participants (12 with ASD, 12 controls) completed a functional magnetic resonance imaging study while performing an attention cuing task with emotional (happy, sad, angry) and neutral faces.

Results: In response to emotional faces, those in the ASD group showed greater right amygdala activation than those in the control group. A preliminary psychophysiological connectivity analysis showed that ASD participants had stronger positive right amygdala and ventromedial prefrontal cortex coupling and weaker positive right amygdala and temporal lobe coupling than controls. There were no group differences in the behavioural measure of attention bias to the emotional faces.

Limitations: The small sample size may have affected our ability to detect additional group differences.

Conclusion: When attention bias to emotional faces was equivalent between ASD and control groups, ASD was associated with greater amygdala activation. Preliminary analyses showed that ASD participants had stronger connectivity between the amygdala ventromedial prefrontal cortex (a network implicated in emotional modulation) and weaker connectivity between the amygdala and temporal lobe (a pathway involved in the identification of facial expressions, although areas of group differences were generally in a more anterior region of the temporal lobe than what is typically reported for emotional face processing). These alterations in connectivity are consistent with emotion and face processing disturbances in ASD.


Submitted July 16, 2009; Revised Nov. 13, Dec. 4, 2009; Accepted Dec. 7, 2009.

Acknowledgments: This research was supported in part by the National Institutes Health (K22 MH068017 to C.S.M, U19 HD35482 to C.L. and MH066496 to C.L.). We thank Dr. D. Noll for methodological advice, and Dr. S.J. Fromm and K. Newnham for technical support. Data from this study were presented at the International Meeting for Autism Research, London, UK, in May 2008.

Competing interests: None declared for Drs. Monk and Weng and Mr. Kurapati, Ms. Wiggins, Ms. Carrasco and Ms. Maslowsky. Drs. Lord and Risi receive royalties from a publisher of diagnostic instruments described in this paper. They donate all profits generated by the University of Michigan Autism and Communication Disorders Center (UMACC) in regards to this paper and all other UMACC projects to a charity.

Contributors: Dr. Monk designed the study. Drs. Monk, Weng, Risi and Lord and Ms. Wiggins, Carrasco and Maslowsky acquired the data. Dr. Monk wrote the article. All authors analyzed the data, reviewed the article and approved its publication.

DOI: 10.1503/jpn.090085

Correspondence to: Dr. C.S. Monk, Department of Psychology, University of Michigan, 530 Church St., Ann Arbor MI 48109; fax 734 615-0573; csmonk@umich.edu