Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area

Frontiers in Behavioral Neuroscience, vol. 15, pp. 744466

Abstract

Rationale: Face expertise is a pivotal social skill. Developmental prosopagnosia (DP), i.e., the inability to recognize faces without a history of brain damage, affects about 2% of the general population, and is a renowned model system of the face-processing network. Within this network, the right Fusiform Face Area (FFA), is particularly involved in face identity processing and may therefore be a key element in DP. Neural representations within the FFA have been examined with Representational Similarity Analysis (RSA), a data-analytical framework in which multi-unit measures of brain activity are assessed with correlation analysis. Objectives: Our study intended to scrutinize modifications of FFA-activation during face encoding and maintenance based on RSA. Methods: Thirteen participants with DP (23–70 years) and 12 healthy control subjects (19–62 years) participated in a functional MRI study, including morphological MRI, a functional FFA-localizer and a modified Sternberg paradigm probing face memory encoding and maintenance. Memory maintenance of one, two, or four faces represented low, medium, and high memory load. We examined conventional activation differences in response to working memory load and applied RSA to compute individual correlation-matrices on the voxel level. Group correlation-matrices were compared via Donsker’s random walk analysis. Results: On the functional level, increased memory load entailed both a higher absolute FFA-activation level and a higher degree of correlation between activated voxels. Both aspects were deficient in DP. Interestingly, control participants showed a homogeneous degree of correlation for successful trials during the experiment. In DP-participants, correlation levels between FFA-voxels were significantly lower and were less sustained during the experiment. In behavioral terms, DP-participants performed poorer and had longer reaction times in relation to DP-severity. Furthermore, correlation levels were negatively correlated with reaction times for the most demanding high load condition. Conclusion: We suggest that participants with DP fail to generate robust and maintained neural representations in the FFA during face encoding and maintenance, in line with poorer task performance and prolonged reaction times. In DP, alterations of neural coding in the FFA might therefore explain curtailing in working memory and contribute to impaired long-term memory and mental imagery.

Authors 8

1. Alexa Haeger corresponding Aachen Department of Neurology

   Forschungszentrum Jülich · Jülich Aachen Research Alliance · RWTH Aachen University

   Affiliation as printed

   Department of Neurology, RWTH Aachen University, Aachen, Germany

   Forschungszentrum Jülich GmbH, Institute of Neuroscience and Medicine (INM-11), Jülich, Germany

   JARA-BRAIN, Jülich, Germany

   FZJ - Forschungszentrum Jülich GmbH | Centre de recherche de Jülich | Jülich Research Centre (Wilhelm-Johnen-Straße, 52428 Jülich - Germany)

   JARA-BRAIN [Aix-la-Chapelle, Allemagne] (Germany)

   RWTH - Rheinisch-Westfälische Technische Hochschule Aachen University (RWTH Aachen Templergraben 55 52062 Aachen (Hausanschrift) 52056 Aachen (Postanschrift) - Germany)

2. Christophe Pouzat

   Institut de Recherche Mathématique Avancée · Mathématiques Appliquées à Paris 5 · Université Paris Descartes

   Affiliation as printed

   Paris Descartes, MAP5, Paris, France

   IRMA - Institut de Recherche Mathématique Avancée (7 rue René-Descartes, 67084 Strasbourg Cedex, France - France)

   MAP5 - UMR 8145 - Mathématiques Appliquées Paris 5 (UFR Mathématiques et Informatique, 45 rue des Saints-Pères 75270 PARIS CEDEX 06 - France)

3. Volker Luecken Aachen

   RWTH Aachen University

   Affiliation as printed

   RWTH Aachen University, Aachen, Germany

   RWTH - Rheinisch-Westfälische Technische Hochschule Aachen University (RWTH Aachen Templergraben 55 52062 Aachen (Hausanschrift) 52056 Aachen (Postanschrift) - Germany)

4. Karim N’Diaye

   Centre National de la Recherche Scientifique · Inserm · Sorbonne Université · Institut des Sciences Moléculaires · Institut du Cerveau

   Affiliation as printed

   Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France

   ICM - Institut du Cerveau = Paris Brain Institute (47-83 Boulevard de l'Hôpital 75651 Paris Cedex 13 - France)

5. Christian Erich Elger
   Affiliation as printed

   Department of Neurology, Beta Klinik, Bonn, Germany

   BetaKlinik (Bonn - Germany)

6. Ingo Kennerknecht

   University of Münster

   Affiliation as printed

   Institute of Human Genetics, Westfaelische Wilhelms-Universitaet Muenster, Muenster, Germany

   WWU - Westfälische Wilhelms-Universität Münster = University of Münster (Universität Münster Schlossplatz 2 48149 Münster - Germany)

7. Nikolai Axmacher

   Ruhr University Bochum

   Affiliation as printed

   Department of Neuropsychology, Ruhr University Bochum, Bochum, Germany

   RUB - Ruhr University Bochum = Ruhr-Universität Bochum (Germany)

8. Vera Dinkelacker

   Fondation Ophtalmologique Adolphe de Rothschild · Fondation de Rothschild · Hôpital d'Hautepierre · Université de Strasbourg

   Affiliation as printed

   Neurology Department, Hautepierre Hospital, University of Strasbourg, Strasbourg, France

   Rothschild Foundation, Neurology Department, Paris, France

   Hôpital de Hautepierre [Strasbourg] (Avenue Molière 67200 Strasbourg - France)

   Hôpital de la Fondation Ophtalmologique Adolphe de Rothschild [AP-HP] (France)