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

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 F...

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Main Authors: Alexa Haeger, Christophe Pouzat, Volker Luecken, Karim N’Diaye, Christian Elger, Ingo Kennerknecht, Nikolai Axmacher, Vera Dinkelacker
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-11-01
Series:Frontiers in Behavioral Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnbeh.2021.744466/full
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author Alexa Haeger
Alexa Haeger
Alexa Haeger
Christophe Pouzat
Volker Luecken
Karim N’Diaye
Christian Elger
Ingo Kennerknecht
Nikolai Axmacher
Vera Dinkelacker
Vera Dinkelacker
author_facet Alexa Haeger
Alexa Haeger
Alexa Haeger
Christophe Pouzat
Volker Luecken
Karim N’Diaye
Christian Elger
Ingo Kennerknecht
Nikolai Axmacher
Vera Dinkelacker
Vera Dinkelacker
author_sort Alexa Haeger
collection DOAJ
description 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.
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spelling doaj.art-a8688b75c64749159a233b1d478399ce2022-12-21T19:29:56ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532021-11-011510.3389/fnbeh.2021.744466744466Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face AreaAlexa Haeger0Alexa Haeger1Alexa Haeger2Christophe Pouzat3Volker Luecken4Karim N’Diaye5Christian Elger6Ingo Kennerknecht7Nikolai Axmacher8Vera Dinkelacker9Vera Dinkelacker10JARA-BRAIN, Jülich, GermanyForschungszentrum Jülich GmbH, Institute of Neuroscience and Medicine (INM-11), Jülich, GermanyDepartment of Neurology, RWTH Aachen University, Aachen, GermanyParis Descartes, MAP5, Paris, FranceRWTH Aachen University, Aachen, GermanyInstitut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, FranceDepartment of Neurology, Beta Klinik, Bonn, GermanyInstitute of Human Genetics, Westfaelische Wilhelms-Universitaet Muenster, Muenster, GermanyDepartment of Neuropsychology, Ruhr University Bochum, Bochum, Germany0Neurology Department, Hautepierre Hospital, University of Strasbourg, Strasbourg, France1Rothschild Foundation, Neurology Department, Paris, FranceRationale: 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.https://www.frontiersin.org/articles/10.3389/fnbeh.2021.744466/fullprosopagnosiafusiform face area (FFA)perceptionrepresentational similarity analysis (RSA)Donsker’s random walk analysisworking memory
spellingShingle Alexa Haeger
Alexa Haeger
Alexa Haeger
Christophe Pouzat
Volker Luecken
Karim N’Diaye
Christian Elger
Ingo Kennerknecht
Nikolai Axmacher
Vera Dinkelacker
Vera Dinkelacker
Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
Frontiers in Behavioral Neuroscience
prosopagnosia
fusiform face area (FFA)
perception
representational similarity analysis (RSA)
Donsker’s random walk analysis
working memory
title Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
title_full Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
title_fullStr Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
title_full_unstemmed Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
title_short Face Processing in Developmental Prosopagnosia: Altered Neural Representations in the Fusiform Face Area
title_sort face processing in developmental prosopagnosia altered neural representations in the fusiform face area
topic prosopagnosia
fusiform face area (FFA)
perception
representational similarity analysis (RSA)
Donsker’s random walk analysis
working memory
url https://www.frontiersin.org/articles/10.3389/fnbeh.2021.744466/full
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