Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies

Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies

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J Psychiatry Neurosci 2009; 34(6): 418-432

Paolo Fusar-Poli, MD; Anna Placentino, MD; Francesco Carletti, MD; Paola Landi, MD; Paul Allen, PhD; Simon Surguladze, PhD; Francesco Benedetti, PhD; Marta Abbamonte, MD; Roberto Gasparotti, PhD; Francesco Barale, PhD; Jorge Perez, PhD; Philip McGuire, PhD; Pierluigi Politi, PhD

Fusar-Poli, Carletti, Allen, McGuire — Section of Neuroimaging, Department of Psychological Medicine, Institute of Psychiatry, King’s College London, United Kingdom; Fusar-Poli, Landi, Abbamonte, Barale, Politi — Section of Psychiatry, Department of Health Sciences, University of Pavia; Placentino, Perez — Biological Psychiatry Unit and Dual Diagnosis Ward IRCCS, Centro San Giovanni di Dio, Fatebenefratelli, Brescia; Carletti, Gasparotti — Department of Diagnostic Imaging, Neuroradiology Unit, University of Brescia, Italy; Surguladze — Section of Affective Neuroscience, Department of Psychological Medicine, Institute of Psychiatry, King’s College London, United Kingdom; Benedetti — Department of Neuropsychiatric Sciences, Scientific Institute and University Vita-Salute San Raffaele, Milan, Italy.

Abstract

Background: Most of our social interactions involve perception of emotional information from the faces of other people. Furthermore, such emotional processes are thought to be aberrant in a range of clinical disorders, including psychosis and depression. However, the exact neurofunctional maps underlying emotional facial processing are not well defined.

Methods: Two independent researchers conducted separate comprehensive PubMed (1990 to May 2008) searches to find all functional magnetic resonance imaging (fMRI) studies using a variant of the emotional faces paradigm in healthy participants. The search terms were: “fMRI AND happy faces,” “fMRI AND sad faces,” “fMRI AND fearful faces,” “fMRI AND angry faces,” “fMRI AND disgusted faces” and “fMRI AND neutral faces.” We extracted spatial coordinates and inserted them in an electronic database. We performed activation likelihood estimation analysis for voxel-based meta-analyses.

Results: Of the originally identified studies, 105 met our inclusion criteria. The overall database consisted of 1785 brain coordinates that yielded an overall sample of 1600 healthy participants. Quantitative voxel-based meta-analysis of brain activation provided neurofunctional maps for 1) main effect of human faces; 2) main effect of emotional valence; and 3) modulatory effect of age, sex, explicit versus implicit processing and magnetic field strength. Processing of emotional faces was associated with increased activation in a number of visual, limbic, temporoparietal and prefrontal areas; the putamen; and the cerebellum. Happy, fearful and sad faces specifically activated the amygdala, whereas angry or disgusted faces had no effect on this brain region. Furthermore, amygdala sensitivity was greater for fearful than for happy or sad faces. Insular activation was selectively reported during processing of disgusted and angry faces. However, insular sensitivity was greater for disgusted than for angry faces. Conversely, neural response in the visual cortex and cerebellum was observable across all emotional conditions.

Limitations: Although the activation likelihood estimation approach is currently one of the most powerful and reliable meta-analytical methods in neuroimaging research, it is insensitive to effect sizes.

Conclusions: Our study has detailed neurofunctional maps to use as normative references in future fMRI studies of emotional facial processing in psychiatric populations. We found selective differences between neural networks underlying the basic emotions in limbic and insular brain regions.


Submitted Nov. 20, 2008; Revised Apr. 6, Jun. 12, 16, 2009; Accepted Jun. 22, 2009

Acknowledgements: We thank Dr. Angela Laird for her valuable advice with the meta-analytical package.

Competing interests: None declared.

Contributors: Drs. Fusar-Poli, Placentino, Allen, Barale, Perez, McGuire and Politi designed the study. Drs. Fusar-Poli, Carletti, Landi, Abbamonte and Gasparotti acquired the data, which Drs. Fusar-Poli, Surguladze, Benedetti and McGuire analyzed. Drs. Fusar-Poli, Landi and Perez wrote the article, which all other authors reviewed. All authors approved the final version for publication.

Correspondence to: Dr. P. Fusar-Poli, Neuroimaging Section, Division of Psychological Medicine PO67, Institute of Psychiatry, De Crespigny Park 16, SE58AF London UK; fax 44 (0)20 7848 0976; p.fusar@libero.it